Meta-Analysis

. 2018 Nov 21;39(44):3961-3969.

doi: 10.1093/eurheartj/ehy474.

A comprehensive evaluation of the genetic architecture of sudden cardiac arrest

Foram N Ashar¹, Rebecca N Mitchell¹, Christine M Albert², Christopher Newton-Cheh³, Jennifer A Brody⁴, Martina Müller-Nurasyid^{5

6

7

8}, Anna Moes¹, Thomas Meitinger^{8

9

10}, Angel Mak¹¹, Heikki Huikuri¹², M Juhani Junttila¹², Philippe Goyette¹³, Sara L Pulit¹⁴, Raha Pazoki¹⁵, Michael W Tanck¹⁶, Marieke T Blom¹⁷, XiaoQing Zhao¹⁸, Aki S Havulinna¹⁹, Reza Jabbari²⁰, Charlotte Glinge²⁰, Vinicius Tragante²¹, Stefan A Escher²², Aravinda Chakravarti¹, Georg Ehret¹, Josef Coresh²³, Man Li²³, Ronald J Prineas²⁴, Oscar H Franco^{25

26}, Pui-Yan Kwok¹¹, Thomas Lumley²⁷, Florence Dumas²⁸, Barbara McKnight^{4

29}, Jerome I Rotter³⁰, Rozenn N Lemaitre⁴, Susan R Heckbert³¹, Christopher J O'Donnell^{32

33}, Shih-Jen Hwang³³, Jean-Claude Tardif¹³, Martin VanDenburgh², André G Uitterlinden³⁴, Albert Hofman²⁶, Bruno H C Stricker²⁶, Paul I W de Bakker^{35

36}, Paul W Franks²², Jan-Hakan Jansson³⁷, Folkert W Asselbergs^{21

38

39}, Marc K Halushka⁴⁰, Joseph J Maleszewski⁴¹, Jacob Tfelt-Hansen^{20

42}, Thomas Engstrøm^{20

43}, Veikko Salomaa¹⁹, Renu Virmani¹⁸, Frank Kolodgie¹⁸, Arthur A M Wilde⁴⁴, Hanno L Tan⁴⁴, Connie R Bezzina⁴⁴, Mark Eijgelsheim⁴⁵, John D Rioux¹³, Xavier Jouven²⁸, Stefan Kääb^{7

8}, Bruce M Psaty⁴⁶, David S Siscovick⁴⁷, Dan E Arking¹, Nona Sotoodehnia⁴⁸

Affiliations

¹ McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins, 733 N Broadway, Baltimore, MD, USA.
² Divisions of Preventive Medicine and Cardiovascular Medicine, Department of Medicine, Brigham and Women's Hospital, 900 Commonwealth Ave East, 3rd Floor, Boston, MA, USA.
³ Center for Human Genetic Research & Cardiovascular Research Center, Massachusetts General Hospital, 55 Fruit Street, Boston, MA, USA.
⁴ Cardiovascular Health Research Unit, Department of Medicine, University of Washington, 1730 Minor Ave, Seattle, WA, USA.
⁵ Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health, Ingolstädter Landstraße 1, Neuherberg, Germany.
⁶ Chair of Genetic Epidemiology, Institute for Medical Informatics, Biometry and Epidemiology, Faculty of Medicine, Ludwig-Maximilians University, Marchioninistr. 15, Munich, Germany.
⁷ Department of Internal Medicine I (Cardiology), Hospital of the Ludwig-Maximilians-University, Marchioninistr. 15, Munich, Germany.
⁸ DZHK (German Centre for Cardiovascular Research), partner site Munich Heart Alliance, Biedersteiner Strasse 29, Munich, Germany.
⁹ Institute of Human Genetics, Helmholtz Zentrum München - German Research Center for Environmental Health, Ingolstaedter Landstrasse 1, Neuherberg, Germany.
¹⁰ Institute of Human Genetics, Klinikum rechts der Isar, Technische Universität München, Ismaninger Strasse 22, Munich, Germany.
¹¹ Cardiovascular Research Institute and Institute for Human Genetics, University of California, San Francisco, 1550 4th Street, San Francisco, CA, USA.
¹² Research Unit of Internal Medicine, University Hospital and University of Oulu, Kajaaninkatu 50, Oulu, Finland.
¹³ Montreal Heart Institute, Université de Montréal, 5000 rue Bélanger, Montréal, Quebec, Canada.
¹⁴ Department of Genetics, Center for Molecular Medicine, University Medical Centre Utrecht, Heidelberglaan 100, Utrecht, The Netherlands.
¹⁵ Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, St Mary's Hospital, Praed St, Paddington, London, UK.
¹⁶ Department of Clinical Epidemiology, Biostatistics and Bioinformatics, Academic Medical Center, Meibergdreef 9, AZ Amsterdam, The Netherlands.
¹⁷ Department of Clinical and Experimental Cardiology, Heart Center, Academic Medical Center, Meibergdreef 9, AZ Amsterdam, The Netherlands.
¹⁸ CVPath Institute, 19 Firstfield Road, Gaithersburg, MD, USA.
¹⁹ National Institute for Health and Welfare, Mannerheimintie 166, Helsinki, Finland.
²⁰ Department of Cardiology, Rigshospitalet, Inge Lehmanns Vej 7, Copenhagen, Denmark.
²¹ Department of Cardiology, Division Heart & Lungs, University Medical Center Utrecht, University of Utrecht, Heidelberglaan 100, Utrecht, The Netherlands.
²² Lund University Diabetes Centre, Department of Clinical Sciences, Lund University, Barngatan 4, Skånes universitetssjukhus, Malmo, Sweden.
²³ Department of Epidemiology, Johns Hopkins University, 615 N Wolfe Street, Baltimore, MD, USA.
²⁴ Public Health Sciences, Wake Forest University, Medical Center Boulevard, Winston-Salem, NC, USA.
²⁵ Institute of Social and Preventative Medicine, University of Bern, Mittelstrasse 43, Bern, Switzerland.
²⁶ Department of Epidemiology, Erasmus MC, Dr. Molewaterplein 50, GE Rotterdam, The Netherlands.
²⁷ Department of Statistics, University of Auckland, Private Bag 92014, Auckland, New Zealand.
²⁸ Paris Sudden Death Expertise Center, University Paris Descartes, Sorbonne Paris Cité, INSERM U970, 56 rue Leblanc, Paris, France.
²⁹ Department of Biostatistics, University of Washington, F-600, Health Sciences Building 1705 NE Pacific Street, Seattle, WA, USA.
³⁰ The Institute for Translational Genomics and Population Sciences, Departments of Pediatrics and Medicine, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, 1124 W. Carson Street, Torrance, CA, USA.
³¹ Cardiovascular Health Research Unit, Department of Epidemiology, University of Washington, 1959 NE Pacific St, Seattle, WA, USA.
³² NHLBI Framingham Heart Study, 73 Mount Wayte Avenue, Suite #2, Framingham, MA, USA.
³³ Cardiology Section, Department of Medicine, Boston VA Healthcare System, 1400 VFW Parkway, Boston, MA, USA.
³⁴ Erasmus MC University Medical Center, Department of Internal Medicine, Dr. Molewaterplein 40, CD Rotterdam, The Netherlands.
³⁵ Department of Genetics, Center for Molecular Medicine, University Medical Center Utrecht, Heidelberglaan 100, Utrecht, The Netherlands.
³⁶ Department of Epidemiology, Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Heidelberglaan 100, Utrecht, The Netherlands.
³⁷ Department of Public Health and Clinical Medicine, Research Unit Skelleftea, Umea University, University Hospital, Building 1A, 4st, Umea, Sweden.
³⁸ Institute of Cardiovascular Science, Faculty of Population Health Sciences, University College London, 69-75 Chenies Mews, London, UK.
³⁹ Institute of Health Informatics, University College London, 222 Euston Road London, UK.
⁴⁰ Department of Pathology, Division of Cardiovascular Pathology, Johns Hopkins University School of Medicine, 720 Rutland Avenue, Ross Rm 632B, Baltimore, MD, USA.
⁴¹ Department of Laboratory Medicine & Pathology, Mayo Clinic, 3050 Superior Drive, Rochester, MN, USA.
⁴² Department of Forensic Medicine, Faculty of Medical Sciences, University of Copenhagen, Inge Lehmanns Vej 7, Copenhagen, Denmark.
⁴³ Department of Cardiology, University of Lund, Getingevägen 4, Lund, Sweden.
⁴⁴ Amsterdam UMC, University of Amsterdam, Heart Center; Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, AZ, Amsterdam, The Netherlands.
⁴⁵ Department of Nephrology, University Medical Center Groningen, Hanzeplein 1, GZ, Groningen, The Netherlands.
⁴⁶ Cardiovascular Health Research Unit, Departments of Medicine, Epidemiology, and Health Services, University of Washington, 1730 Minor Ave, suite #1360, Seattle, WA, USA.
⁴⁷ The New York Academy of Medicine, 1216 5th Ave, New York, New York, USA.
⁴⁸ Cardiovascular Health Research Unit, Division of Cardiology, Departments of Medicine and Epidemiology, University of Washington, 1730 Minor Ave, Seattle, WA, USA.

PMID: 30169657
PMCID: PMC6247663
DOI: 10.1093/eurheartj/ehy474

Meta-Analysis

A comprehensive evaluation of the genetic architecture of sudden cardiac arrest

Foram N Ashar et al. Eur Heart J. 2018.

. 2018 Nov 21;39(44):3961-3969.

doi: 10.1093/eurheartj/ehy474.

Authors

Affiliations

¹ McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins, 733 N Broadway, Baltimore, MD, USA.
² Divisions of Preventive Medicine and Cardiovascular Medicine, Department of Medicine, Brigham and Women's Hospital, 900 Commonwealth Ave East, 3rd Floor, Boston, MA, USA.
³ Center for Human Genetic Research & Cardiovascular Research Center, Massachusetts General Hospital, 55 Fruit Street, Boston, MA, USA.
⁴ Cardiovascular Health Research Unit, Department of Medicine, University of Washington, 1730 Minor Ave, Seattle, WA, USA.
⁵ Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health, Ingolstädter Landstraße 1, Neuherberg, Germany.
⁶ Chair of Genetic Epidemiology, Institute for Medical Informatics, Biometry and Epidemiology, Faculty of Medicine, Ludwig-Maximilians University, Marchioninistr. 15, Munich, Germany.
⁷ Department of Internal Medicine I (Cardiology), Hospital of the Ludwig-Maximilians-University, Marchioninistr. 15, Munich, Germany.
⁸ DZHK (German Centre for Cardiovascular Research), partner site Munich Heart Alliance, Biedersteiner Strasse 29, Munich, Germany.
⁹ Institute of Human Genetics, Helmholtz Zentrum München - German Research Center for Environmental Health, Ingolstaedter Landstrasse 1, Neuherberg, Germany.
¹⁰ Institute of Human Genetics, Klinikum rechts der Isar, Technische Universität München, Ismaninger Strasse 22, Munich, Germany.
¹¹ Cardiovascular Research Institute and Institute for Human Genetics, University of California, San Francisco, 1550 4th Street, San Francisco, CA, USA.
¹² Research Unit of Internal Medicine, University Hospital and University of Oulu, Kajaaninkatu 50, Oulu, Finland.
¹³ Montreal Heart Institute, Université de Montréal, 5000 rue Bélanger, Montréal, Quebec, Canada.
¹⁴ Department of Genetics, Center for Molecular Medicine, University Medical Centre Utrecht, Heidelberglaan 100, Utrecht, The Netherlands.
¹⁵ Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, St Mary's Hospital, Praed St, Paddington, London, UK.
¹⁶ Department of Clinical Epidemiology, Biostatistics and Bioinformatics, Academic Medical Center, Meibergdreef 9, AZ Amsterdam, The Netherlands.
¹⁷ Department of Clinical and Experimental Cardiology, Heart Center, Academic Medical Center, Meibergdreef 9, AZ Amsterdam, The Netherlands.
¹⁸ CVPath Institute, 19 Firstfield Road, Gaithersburg, MD, USA.
¹⁹ National Institute for Health and Welfare, Mannerheimintie 166, Helsinki, Finland.
²⁰ Department of Cardiology, Rigshospitalet, Inge Lehmanns Vej 7, Copenhagen, Denmark.
²¹ Department of Cardiology, Division Heart & Lungs, University Medical Center Utrecht, University of Utrecht, Heidelberglaan 100, Utrecht, The Netherlands.
²² Lund University Diabetes Centre, Department of Clinical Sciences, Lund University, Barngatan 4, Skånes universitetssjukhus, Malmo, Sweden.
²³ Department of Epidemiology, Johns Hopkins University, 615 N Wolfe Street, Baltimore, MD, USA.
²⁴ Public Health Sciences, Wake Forest University, Medical Center Boulevard, Winston-Salem, NC, USA.
²⁵ Institute of Social and Preventative Medicine, University of Bern, Mittelstrasse 43, Bern, Switzerland.
²⁶ Department of Epidemiology, Erasmus MC, Dr. Molewaterplein 50, GE Rotterdam, The Netherlands.
²⁷ Department of Statistics, University of Auckland, Private Bag 92014, Auckland, New Zealand.
²⁸ Paris Sudden Death Expertise Center, University Paris Descartes, Sorbonne Paris Cité, INSERM U970, 56 rue Leblanc, Paris, France.
²⁹ Department of Biostatistics, University of Washington, F-600, Health Sciences Building 1705 NE Pacific Street, Seattle, WA, USA.
³⁰ The Institute for Translational Genomics and Population Sciences, Departments of Pediatrics and Medicine, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, 1124 W. Carson Street, Torrance, CA, USA.
³¹ Cardiovascular Health Research Unit, Department of Epidemiology, University of Washington, 1959 NE Pacific St, Seattle, WA, USA.
³² NHLBI Framingham Heart Study, 73 Mount Wayte Avenue, Suite #2, Framingham, MA, USA.
³³ Cardiology Section, Department of Medicine, Boston VA Healthcare System, 1400 VFW Parkway, Boston, MA, USA.
³⁴ Erasmus MC University Medical Center, Department of Internal Medicine, Dr. Molewaterplein 40, CD Rotterdam, The Netherlands.
³⁵ Department of Genetics, Center for Molecular Medicine, University Medical Center Utrecht, Heidelberglaan 100, Utrecht, The Netherlands.
³⁶ Department of Epidemiology, Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Heidelberglaan 100, Utrecht, The Netherlands.
³⁷ Department of Public Health and Clinical Medicine, Research Unit Skelleftea, Umea University, University Hospital, Building 1A, 4st, Umea, Sweden.
³⁸ Institute of Cardiovascular Science, Faculty of Population Health Sciences, University College London, 69-75 Chenies Mews, London, UK.
³⁹ Institute of Health Informatics, University College London, 222 Euston Road London, UK.
⁴⁰ Department of Pathology, Division of Cardiovascular Pathology, Johns Hopkins University School of Medicine, 720 Rutland Avenue, Ross Rm 632B, Baltimore, MD, USA.
⁴¹ Department of Laboratory Medicine & Pathology, Mayo Clinic, 3050 Superior Drive, Rochester, MN, USA.
⁴² Department of Forensic Medicine, Faculty of Medical Sciences, University of Copenhagen, Inge Lehmanns Vej 7, Copenhagen, Denmark.
⁴³ Department of Cardiology, University of Lund, Getingevägen 4, Lund, Sweden.
⁴⁴ Amsterdam UMC, University of Amsterdam, Heart Center; Department of Clinical and Experimental Cardiology, Amsterdam Cardiovascular Sciences, Meibergdreef 9, AZ, Amsterdam, The Netherlands.
⁴⁵ Department of Nephrology, University Medical Center Groningen, Hanzeplein 1, GZ, Groningen, The Netherlands.
⁴⁶ Cardiovascular Health Research Unit, Departments of Medicine, Epidemiology, and Health Services, University of Washington, 1730 Minor Ave, suite #1360, Seattle, WA, USA.
⁴⁷ The New York Academy of Medicine, 1216 5th Ave, New York, New York, USA.
⁴⁸ Cardiovascular Health Research Unit, Division of Cardiology, Departments of Medicine and Epidemiology, University of Washington, 1730 Minor Ave, Seattle, WA, USA.

PMID: 30169657
PMCID: PMC6247663
DOI: 10.1093/eurheartj/ehy474

Abstract

Aims: Sudden cardiac arrest (SCA) accounts for 10% of adult mortality in Western populations. We aim to identify potential loci associated with SCA and to identify risk factors causally associated with SCA.

Methods and results: We carried out a large genome-wide association study (GWAS) for SCA (n = 3939 cases, 25 989 non-cases) to examine common variation genome-wide and in candidate arrhythmia genes. We also exploited Mendelian randomization (MR) methods using cross-trait multi-variant genetic risk score associations (GRSA) to assess causal relationships of 18 risk factors with SCA. No variants were associated with SCA at genome-wide significance, nor were common variants in candidate arrhythmia genes associated with SCA at nominal significance. Using cross-trait GRSA, we established genetic correlation between SCA and (i) coronary artery disease (CAD) and traditional CAD risk factors (blood pressure, lipids, and diabetes), (ii) height and BMI, and (iii) electrical instability traits (QT and atrial fibrillation), suggesting aetiologic roles for these traits in SCA risk.

Conclusions: Our findings show that a comprehensive approach to the genetic architecture of SCA can shed light on the determinants of a complex life-threatening condition with multiple influencing factors in the general population. The results of this genetic analysis, both positive and negative findings, have implications for evaluating the genetic architecture of patients with a family history of SCA, and for efforts to prevent SCA in high-risk populations and the general community.

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Figures

**Figure 1**
Genetic Risk Score Association (GRSA) estimation. The plot (A) illustrates the process by which the QT-SCA Genetic Risk Score Association is calculated using SNPs associated with QT at P < 5 × 10⁻⁸. The points represent the effect of each SNP on QT (in units of standard deviation of QT) on the x-axis and the log odds effect on sudden cardiac arrest risk (corresponding 95% confidence intervals in grey) on the y-axis. The estimate of the genetic risk score association is the slope of the zero-intercept weighted regression line (solid red line). For the Genetic Risk Score Association used in our analyses, the model contains a genome-wide LD-pruned SNP set (details in Methods section). The top directed acyclic graph (B) represents a scenario in which the trait of interest has a causal effect on the outcome. If the Genetic Risk Score Association, comprised of trait-associated variants (e.g. QT), has a significant effect on the outcome (e.g. sudden cardiac arrest), it supports a causal role for the trait on the outcome. The bottom directed acyl graph (C) presents the case where an association is observed between the trait and outcome, but the Genetic Risk Score Association comprised of trait-associated variants is not significantly associated with the outcome, suggesting that the observational association is likely being mediated by a confounding variable and the trait does not have a causal impact on the outcome.

**Figure 2**
Genetic Risk Scores Association (GRSA) estimates for sudden cardiac arrest. These data points represent the exponentiated Genetic Risk Score Association estimates of 18 traits on sudden cardiac arrest (SCA) and corresponding 95% confidence interval values. The Genetic Risk Score Association estimates in the top panel for the binary traits are in log odds units. Values in bottom panel are in SD units of the quantitative traits. Genetic Risk Score Association estimates and significance are derived from SNPs associated with each trait at P < 5 × 10⁻⁸. The significance of the GRSA_GWS estimates (false discovery rate adjusted P_GWS) are represented as ‘*’ for P < 0.05, ‘**’ for P < 0.01, and ‘***’ for P < 0.001. The significance of the secondary analysis using GRSA_max estimates (false discovery rate adjusted permuted P_max) are represented as ‘+’ for P < 0.05, ‘++’ for P < 0.01 and ‘+++’ for P < 0.001. For details on values of Genetic Risk Score Association estimates and P-values, see Supplementary material online, *Tables S8* and *S9.* AF, atrial fibrillation; BMI, body mass index; CAD, coronary artery disease; DBP, diastolic blood pressure; FGadjBMI, fasting glucose adjusted for BMI; FIadjBMI, fasting insulin adjusted for BMI; HDL, high-density lipoproteins; HR, heart rate; LDL, low-density lipoproteins; QRS, QRS interval; QT, QT interval; SBP, systolic blood pressure; TCH, total cholesterol; TG, triglycerides; T2D, type 2 diabetes; WCadjBMI, waist circumference adjusted for BMI; WHRadBMI, waist-to-hip ratio adjusted for BMI.

**Figure 3**
Comparison of Genetic Risk Score Association for sudden cardiac arrest and coronary artery disease. These data represent exponentiated Genetic Risk Score Associations of all 17 traits. Genetic Risk Score Association estimates for sudden cardiac arrest and coronary artery disease, are plotted in orange and teal, respectively. Bars around the estimates represent the 95% confidence interval. The Genetic Risk Score Association estimates in the top panel for the binary traits are in log odds units. Values in bottom panel are in SD units of the quantitative traits. The level of significance for 1 degree of freedom Wald test of difference in GRSA_GWS estimates between sudden cardiac arrest and coronary artery disease is represented ‘*’ for P < 0.05, ‘**’ for P < 0.01, and ‘***’ for P < 0.001. AF, atrial fibrillation; BMI, body mass index; DBP, diastolic blood pressure; FGadjBMI, fasting glucose adjusted for BMI; FIadjBMI, fasting insulin adjusted for BMI; HDL, high-density lipoproteins; HR, heart rate; LDL, low-density lipoproteins; QRS, QRS interval; QT, QT interval; SBP, systolic blood pressure; TCH, total cholesterol; TG, triglycerides; T2D, type 2 diabetes; WCadjBMI, waist circumference adjusted for BMI; WHRadBMI, waist-to-hip ratio adjusted for BMI.

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Comment in

Can genetics predict risk for sudden cardiac death? The relentless search for the Holy Grail.
Schwartz PJ, Gentilini D. Schwartz PJ, et al. Eur Heart J. 2018 Nov 21;39(44):3970-3972. doi: 10.1093/eurheartj/ehy508. Eur Heart J. 2018. PMID: 30188985 No abstract available.

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A comprehensive evaluation of the genetic architecture of sudden cardiac arrest

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A comprehensive evaluation of the genetic architecture of sudden cardiac arrest

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