Dyslipidemia, inflammation, calcification, and adiposity in aortic stenosis: a genome-wide study

doi:10.1093/eurheartj/ehad142

Meta-Analysis

. 2023 Jun 1;44(21):1927-1939.

doi: 10.1093/eurheartj/ehad142.

Dyslipidemia, inflammation, calcification, and adiposity in aortic stenosis: a genome-wide study

Hao Yu Chen^{1

2}, Christian Dina³, Aeron M Small⁴, Christian M Shaffer⁵, Rebecca T Levinson⁵, Anna Helgadóttir⁶, Romain Capoulade³, Hans Markus Munter⁷, Andreas Martinsson^{8

9}, Benjamin J Cairns¹⁰, Linea C Trudsø¹¹, Mary Hoekstra^{1

2}, Hannah A Burr^{1

2}, Thomas W Marsh^{2

12}, Scott M Damrauer¹³, Line Dufresne², Solena Le Scouarnec³, David Messika-Zeitoun^{14

15}, Dilrini K Ranatunga¹⁶, Rachel A Whitmer¹⁷, Amélie Bonnefond^{18

19}, Garðar Sveinbjornsson⁶, Ragnar Daníelsen²⁰, David O Arnar^{6

20

21}, Gudmundur Thorgeirsson^{6

21}, Unnur Thorsteinsdottir^{6

21}, Daníel F Gudbjartsson^{6

22}, Hilma Hólm⁶, Jonas Ghouse¹¹, Morten Salling Olesen¹¹, Alex H Christensen^{11

23}, Susan Mikkelsen²⁴, Rikke Louise Jacobsen²⁵, Joseph Dowsett²⁵, Ole Birger Vesterager Pedersen²⁶, Christian Erikstrup^{24

27}, Sisse R Ostrowski^{25

28}; Regeneron Genetics Center; Christopher J O'Donnell²⁹, Matthew J Budoff³⁰, Vilmundur Gudnason³¹, Wendy S Post³², Jerome I Rotter³³, Mark Lathrop^{7

12}, Henning Bundgaard³⁴, Bengt Johansson³⁵, Johan Ljungberg³⁵, Ulf Näslund³⁵, Thierry Le Tourneau³, J Gustav Smith^{8

36

9}, Quinn S Wells⁵, Stefan Söderberg³⁵, Kári Stefánsson^{6

21}, Jean-Jacques Schott³, Daniel J Rader³⁷, Robert Clarke¹⁰, James C Engert^{1

2

12}, George Thanassoulis^{1

2}

Affiliations

¹ Division of Experimental Medicine, McGill University, 1001 Decarie Blvd., Room EM1.2218, Montreal, Quebec H4A 3J1, Canada.
² Preventive and Genomic Cardiology, McGill University Health Centre and Research Institute, 1001 Decarie Blvd., Room D05.5120, Montreal, Quebec H4A 3J1, Canada.
³ Nantes Université, CHU Nantes, CNRS, INSERM, l'institut du thorax, 8 Quai Moncousu, Nantes F-44000, France.
⁴ Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, USA.
⁵ Vanderbilt Translational and Clinical Cardiovascular Research Center, Vanderbilt University Medical Center, Nashville, USA.
⁶ deCODE genetics/Amgen Inc., Reykjavik, Iceland.
⁷ McGill University and Genome Quebec Innovation Centre, Montreal, Canada.
⁸ Department of Cardiology, Clinical Sciences, Lund University, Sweden and Skåne University Hospital, Lund, Sweden.
⁹ The Wallenberg Laboratory/Department of Molecular and Clinical Medicine, Institute of Medicine, Gothenburg University and the Department of Cardiology, Sahlgrenska University Hospital, Gothenburg, Sweden.
¹⁰ MRC Population Health Research Unit, Clinical Trial Service Unit and Epidemiological Studies Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.
¹¹ Laboratory for Molecular Cardiology, Department of Cardiology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
¹² Department of Human Genetics, McGill University, Montreal, Canada.
¹³ Department of Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, USA.
¹⁴ Department of Cardiology, Assistance Publique - Hôpitaux de Paris, Bichat Hospital, Paris, France.
¹⁵ Division of Cardiology, University of Ottawa Heart Institute, Ottawa, Ontario, Canada.
¹⁶ Division of Research, Kaiser Permanente of Northern California, Oakland, USA.
¹⁷ Department of Public Health Sciences, University of California Davis, Davis, USA.
¹⁸ University Lille, Inserm, CNRS, CHU Lille, Institut Pasteur de Lille, UMR1283-8199 EGID, Lille, France.
¹⁹ Department of Metabolism, Imperial College London, London, UK.
²⁰ Internal Medicine and Emergency Services, Landspitali-The National University Hospital of Iceland, Reykjavik, Iceland.
²¹ School of Health Sciences, Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
²² School of Engineering and Natural Sciences, University of Iceland, Reykjavik, Iceland.
²³ Department of Cardiology, Herlev-Gentofte Hospital, Copenhagen, Denmark.
²⁴ Department of Clinical Immunology, Aarhus University Hospital, Aarhus, Denmark.
²⁵ Department of Clinical Immunology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
²⁶ Department of Clinical Immunology, Zealand University Hospital, Naestved, Denmark.
²⁷ Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.
²⁸ Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
²⁹ National Heart, Lung, and Blood Institute's and Boston University's Framingham Heart Study, Boston, USA.
³⁰ The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center, Torrance, USA.
³¹ Faculty of Medicine, University of Iceland, Reykjavík, Iceland.
³² Division of Cardiology, Department of Medicine, The Johns Hopkins University School of Medicine, Baltimore, USA.
³³ The Institute for Translational Genomics and Population Sciences, Department of Pediatrics, The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center, Torrance, USA.
³⁴ Department of Cardiology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
³⁵ Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden.
³⁶ Wallenberg Center for Molecular Medicine and Lund University Diabetes Center, Lund, Sweden.
³⁷ Departments of Genetics and Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, USA.

PMID: 37038246
PMCID: PMC10232274
DOI: 10.1093/eurheartj/ehad142

Meta-Analysis

Dyslipidemia, inflammation, calcification, and adiposity in aortic stenosis: a genome-wide study

Hao Yu Chen et al. Eur Heart J. 2023.

. 2023 Jun 1;44(21):1927-1939.

doi: 10.1093/eurheartj/ehad142.

Authors

Affiliations

¹ Division of Experimental Medicine, McGill University, 1001 Decarie Blvd., Room EM1.2218, Montreal, Quebec H4A 3J1, Canada.
² Preventive and Genomic Cardiology, McGill University Health Centre and Research Institute, 1001 Decarie Blvd., Room D05.5120, Montreal, Quebec H4A 3J1, Canada.
³ Nantes Université, CHU Nantes, CNRS, INSERM, l'institut du thorax, 8 Quai Moncousu, Nantes F-44000, France.
⁴ Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, USA.
⁵ Vanderbilt Translational and Clinical Cardiovascular Research Center, Vanderbilt University Medical Center, Nashville, USA.
⁶ deCODE genetics/Amgen Inc., Reykjavik, Iceland.
⁷ McGill University and Genome Quebec Innovation Centre, Montreal, Canada.
⁸ Department of Cardiology, Clinical Sciences, Lund University, Sweden and Skåne University Hospital, Lund, Sweden.
⁹ The Wallenberg Laboratory/Department of Molecular and Clinical Medicine, Institute of Medicine, Gothenburg University and the Department of Cardiology, Sahlgrenska University Hospital, Gothenburg, Sweden.
¹⁰ MRC Population Health Research Unit, Clinical Trial Service Unit and Epidemiological Studies Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.
¹¹ Laboratory for Molecular Cardiology, Department of Cardiology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
¹² Department of Human Genetics, McGill University, Montreal, Canada.
¹³ Department of Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, USA.
¹⁴ Department of Cardiology, Assistance Publique - Hôpitaux de Paris, Bichat Hospital, Paris, France.
¹⁵ Division of Cardiology, University of Ottawa Heart Institute, Ottawa, Ontario, Canada.
¹⁶ Division of Research, Kaiser Permanente of Northern California, Oakland, USA.
¹⁷ Department of Public Health Sciences, University of California Davis, Davis, USA.
¹⁸ University Lille, Inserm, CNRS, CHU Lille, Institut Pasteur de Lille, UMR1283-8199 EGID, Lille, France.
¹⁹ Department of Metabolism, Imperial College London, London, UK.
²⁰ Internal Medicine and Emergency Services, Landspitali-The National University Hospital of Iceland, Reykjavik, Iceland.
²¹ School of Health Sciences, Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
²² School of Engineering and Natural Sciences, University of Iceland, Reykjavik, Iceland.
²³ Department of Cardiology, Herlev-Gentofte Hospital, Copenhagen, Denmark.
²⁴ Department of Clinical Immunology, Aarhus University Hospital, Aarhus, Denmark.
²⁵ Department of Clinical Immunology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
²⁶ Department of Clinical Immunology, Zealand University Hospital, Naestved, Denmark.
²⁷ Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.
²⁸ Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
²⁹ National Heart, Lung, and Blood Institute's and Boston University's Framingham Heart Study, Boston, USA.
³⁰ The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center, Torrance, USA.
³¹ Faculty of Medicine, University of Iceland, Reykjavík, Iceland.
³² Division of Cardiology, Department of Medicine, The Johns Hopkins University School of Medicine, Baltimore, USA.
³³ The Institute for Translational Genomics and Population Sciences, Department of Pediatrics, The Lundquist Institute for Biomedical Innovation at Harbor-UCLA Medical Center, Torrance, USA.
³⁴ Department of Cardiology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
³⁵ Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden.
³⁶ Wallenberg Center for Molecular Medicine and Lund University Diabetes Center, Lund, Sweden.
³⁷ Departments of Genetics and Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, USA.

PMID: 37038246
PMCID: PMC10232274
DOI: 10.1093/eurheartj/ehad142

Abstract

Aims: Although highly heritable, the genetic etiology of calcific aortic stenosis (AS) remains incompletely understood. The aim of this study was to discover novel genetic contributors to AS and to integrate functional, expression, and cross-phenotype data to identify mechanisms of AS.

Methods and results: A genome-wide meta-analysis of 11.6 million variants in 10 cohorts involving 653 867 European ancestry participants (13 765 cases) was performed. Seventeen loci were associated with AS at P ≤ 5 × 10-8, of which 15 replicated in an independent cohort of 90 828 participants (7111 cases), including CELSR2-SORT1, NLRP6, and SMC2. A genetic risk score comprised of the index variants was associated with AS [odds ratio (OR) per standard deviation, 1.31; 95% confidence interval (CI), 1.26-1.35; P = 2.7 × 10-51] and aortic valve calcium (OR per standard deviation, 1.22; 95% CI, 1.08-1.37; P = 1.4 × 10-3), after adjustment for known risk factors. A phenome-wide association study indicated multiple associations with coronary artery disease, apolipoprotein B, and triglycerides. Mendelian randomization supported a causal role for apolipoprotein B-containing lipoprotein particles in AS (OR per g/L of apolipoprotein B, 3.85; 95% CI, 2.90-5.12; P = 2.1 × 10-20) and replicated previous findings of causality for lipoprotein(a) (OR per natural logarithm, 1.20; 95% CI, 1.17-1.23; P = 4.8 × 10-73) and body mass index (OR per kg/m2, 1.07; 95% CI, 1.05-1.9; P = 1.9 × 10-12). Colocalization analyses using the GTEx database identified a role for differential expression of the genes LPA, SORT1, ACTR2, NOTCH4, IL6R, and FADS.

Conclusion: Dyslipidemia, inflammation, calcification, and adiposity play important roles in the etiology of AS, implicating novel treatments and prevention strategies.

Keywords: Aortic stenosis; Gene expression; Genetic risk score; Genome-wide association study; Mendelian randomization; Phenome-wide association study.

PubMed Disclaimer

Conflict of interest statement

Conflict of interest Scott M. Damrauer receives research support (to the University of Pennsylvania) from RenalytixAI and personal fees from Caico Ibs, both outside the scope of the present work. SMD is also named as a co-inventor on a government-owned US Patent application related to the use of genetic risk prediction for venous thromboembolic disease filed by the US Department of Veterans Affairs in accordance with Federal regulatory requirements. SMD is named as a co-inventor on a Government-owned US Patent application related to the use of PDE3B inhibition for preventing cardiovascular disease filed by the US Department of Veterans Affairs in accordance with Federal regulatory requirements. Stefan Söderberg has received speaker honoraria and consulting fees from Actelion Ltd. George Thanassoulis has received consulting fees from Ionis Pharmaceuticals and has participated in advisory boards for Amgen, Sanofi, Novartis, HLS Therapeutics and Silence. Morten Salling Olesen has received 5.000.000 dkrfra Sundhedsdonationer.Journalnr. 2022-0243. David O. Arnar has received travel support from Pfizer to attend the ESC 2022 Scientific Meeting in Barcelona and has stock options in Sidekick Health Digital Therapeutics. Henning Bundgaard has received lecture fees from Amgen, MSD, Sanofi-Avensis, BMS and grants from NordForsk, Innovation Fond, Denmark, The Capital Regions Research Foundation. Alex Hoerby Christensen—Novo Nordisk Foundation NNF20OC0065799. Romaine Capoulade has received an Honorarium for one lecture from Novartis. Robert Clarke has received support from BAYER (China Kadoorie Biobank). Unnur Thorsteinsdottir’s research is funded by deCODE genetics/Amgen. Daniel F. Gudbjartsson receives funds from deCODE Genetics/Amgen. Until 1 June 2022, Gudmundur Thorgeirsson was a part time employee of deCode Genetics that is owned by Amgen. Hilma Holm is an employee of deCODE genetics/Amgen Inc. Anna Helgadottir is an employee of deCODE genetics/Amgen Inc.

Figures

**Structured Graphical Abstract**
Genetic etiology of aortic stenosis. This study meta-analyzed 13 765 AS cases vs. 640 102 controls and confirmed 15 genetic loci associated with AS. Downstream analyses implicated additional candidate genes involved in dyslipidemia, inflammation, calcification, and adiposity. The Manhattan plot shows variants with P ≥ 1 × 10⁻²⁵, for improved visualization. Genetic loci in grey were previously identified, and those in gold are new discoveries. Abbreviations: AS, aortic stenosis; GWAS, genome-wide association study; LDL, low-density lipoprotein.

**Figure 1**
Design of the genome-wide meta-analysis and follow-up analyses. Abbreviations: ANNOVAR, Annotate Variation; CADD, Combined Annotation Dependent Depletion; DANN, Deleterious Annotation of genetic variants using Neural Networks; EIGEN-PC, Eigen-Principal Component; FANTOM5, Functional Annotation of the Mammalian Genome version 5; FATHMM-MKL, Functional Analysis Through Hidden Markov Models-Multiple Kernel Learning; GCTA COJO, Genome-wide Complex Trait Analysis Conditional and Joint Association Analysis; GIGSEA, Genotype Imputed Gene Set Enrichment Analysis; GO, Gene Ontology; GTEx, Genotype-Tissue Expression project; KEGG, Kyoto Encyclopedia of Genes and Genomics; LDSC, Linkage Disequilibrium Score Regression; LINSIGHT, Linear INSIGHT; MAGMA, Multi-marker Analysis of Genomic Annotation; UCSC, University of California Santa Cruz Genome Browser.

**Figure 2**
P for the association of 11 591 806 variants with aortic stenosis in the meta-analysis. The inset shows all associations, while the main plot shows variants with P ≥ 1 × 10⁻²⁵, for improved visualization. Genetic loci in grey were previously identified and those in gold are new discoveries.

**Figure 3**
Association of aortic stenosis variants with biomarkers, physiological measurements, and diseases. Variants were ordered to reflect similarity in their associations with traits and vice versa. The strength and direction of associations are represented by cells of different colors, with blue cells indicating positive effects on the odds of aortic stenosis and red cells indicating inverse associations. For ease of visualization, Z statistics >5 or less than −5 were rounded to 5 and −5, respectively.

See this image and copyright information in PMC

Comment in

The journey towards identification of actionable molecular pathways in calcific aortic valve stenosis.
Thériault S, Mathieu P, Bossé Y. Thériault S, et al. Eur Heart J. 2023 Jun 1;44(21):1940-1942. doi: 10.1093/eurheartj/ehad134. Eur Heart J. 2023. PMID: 37042229 No abstract available.

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References

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1. Danielsen R, Aspelund T, Harris TB, Gudnason V. The prevalence of aortic stenosis in the elderly in Iceland and predictions for the coming decades: the AGES-Reykjavik study. Int J Cardiol 2014;176:916–922. 10.1016/j.ijcard.2014.08.053 - DOI - PMC - PubMed
1. Vahanian A, Beyersdorf F, Praz F, Milojevic M, Baldus S, Bauersachs J, et al. . 2021 ESC/EACTS guidelines for the management of valvular heart disease. Eur Heart J 2022;43:561–632. 10.1093/eurheartj/ehab395 - DOI - PubMed
1. Members WC, Otto CM, Nishimura RA, Bonow RO, Carabello BA, Erwin JP III, et al. . 2020 ACC/AHA guideline for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. J Am Coll Cardiol 2021;77:e25–e197. 10.1016/j.jacc.2020.11.018 - DOI - PubMed
1. Martinsson A, Li X, Zoller B, Andell P, Andersson C, Sundquist K, et al. . Familial aggregation of aortic valvular stenosis: a nationwide study of sibling risk. Circ Cardiovasc Genet 2017;10:e001742. 10.1161/CIRCGENETICS.117.001742 - DOI - PMC - PubMed

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[1] Andell P, Li X, Martinsson A, Andersson C, Stagmo M, Zoller B, et al. . Epidemiology of valvular heart disease in a Swedish nationwide hospital-based register study. Heart 2017;103:1696–1703. 10.1136/heartjnl-2016-310894 - DOI - PMC - PubMed

[2] Andell P, Li X, Martinsson A, Andersson C, Stagmo M, Zoller B, et al. . Epidemiology of valvular heart disease in a Swedish nationwide hospital-based register study. Heart 2017;103:1696–1703. 10.1136/heartjnl-2016-310894 - DOI - PMC - PubMed

[3] Danielsen R, Aspelund T, Harris TB, Gudnason V. The prevalence of aortic stenosis in the elderly in Iceland and predictions for the coming decades: the AGES-Reykjavik study. Int J Cardiol 2014;176:916–922. 10.1016/j.ijcard.2014.08.053 - DOI - PMC - PubMed

[4] Danielsen R, Aspelund T, Harris TB, Gudnason V. The prevalence of aortic stenosis in the elderly in Iceland and predictions for the coming decades: the AGES-Reykjavik study. Int J Cardiol 2014;176:916–922. 10.1016/j.ijcard.2014.08.053 - DOI - PMC - PubMed

[5] Vahanian A, Beyersdorf F, Praz F, Milojevic M, Baldus S, Bauersachs J, et al. . 2021 ESC/EACTS guidelines for the management of valvular heart disease. Eur Heart J 2022;43:561–632. 10.1093/eurheartj/ehab395 - DOI - PubMed

[6] Vahanian A, Beyersdorf F, Praz F, Milojevic M, Baldus S, Bauersachs J, et al. . 2021 ESC/EACTS guidelines for the management of valvular heart disease. Eur Heart J 2022;43:561–632. 10.1093/eurheartj/ehab395 - DOI - PubMed

[7] Members WC, Otto CM, Nishimura RA, Bonow RO, Carabello BA, Erwin JP III, et al. . 2020 ACC/AHA guideline for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. J Am Coll Cardiol 2021;77:e25–e197. 10.1016/j.jacc.2020.11.018 - DOI - PubMed

[8] Members WC, Otto CM, Nishimura RA, Bonow RO, Carabello BA, Erwin JP III, et al. . 2020 ACC/AHA guideline for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. J Am Coll Cardiol 2021;77:e25–e197. 10.1016/j.jacc.2020.11.018 - DOI - PubMed

[9] Martinsson A, Li X, Zoller B, Andell P, Andersson C, Sundquist K, et al. . Familial aggregation of aortic valvular stenosis: a nationwide study of sibling risk. Circ Cardiovasc Genet 2017;10:e001742. 10.1161/CIRCGENETICS.117.001742 - DOI - PMC - PubMed

[10] Martinsson A, Li X, Zoller B, Andell P, Andersson C, Sundquist K, et al. . Familial aggregation of aortic valvular stenosis: a nationwide study of sibling risk. Circ Cardiovasc Genet 2017;10:e001742. 10.1161/CIRCGENETICS.117.001742 - DOI - PMC - PubMed

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Dyslipidemia, inflammation, calcification, and adiposity in aortic stenosis: a genome-wide study

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Dyslipidemia, inflammation, calcification, and adiposity in aortic stenosis: a genome-wide study

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