Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variants

Background: Hypertrophic cardiomyopathy (HCM) is a genetically heterogeneous disorder linked primarily to rare variants in sarcomeric genes, although recently certain nonsarcomeric genes have emerged as important contributors. Nonmendelian genetic variants with reproducible moderate-effect sizes and...

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Autores: García Hernandez, Soledad, De la Higuera Romero, Luis, Fernandez, Adrian, Luisa Peña Peña, Maria, Mora Ayestaran, Nerea, Basurte Elorz, María Teresa, Larrañaga Moreira, Jose María, Cárdenas Reyes, Ivonne, Villacorta, Eduardo, Valverde Gómez, Maria, Baustista-Paves, Alicia, Veira Villanueva, Elena, Ortiz Genga, Martín, Lipov, Alex, Brogger, Noel, Sabater Molina, María, Moreno Escobar, Eduardo, Ruiz Guerrero, Luis Javier, Syrris, Petros, Piqueras Flores, Jesús
Tipo de recurso: artículo
Fecha de publicación:2025
País:España
Institución:Universidad de Cantabria (UC)
Repositorio:UCrea Repositorio Abierto de la Universidad de Cantabria
Idioma:inglés
OAI Identifier:oai:repositorio.unican.es:10902/38807
Acceso en línea:https://hdl.handle.net/10902/38807
Access Level:acceso abierto
Palabra clave:Cardiomyopathy
Hypertrophic
Genetic predisposition to disease
Genetic testing
Genetic variation
Inheritance patterns
Risk factors
Penetrence
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oai_identifier_str oai:repositorio.unican.es:10902/38807
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variants
title Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variants
spellingShingle Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variants
García Hernandez, Soledad
Cardiomyopathy
Hypertrophic
Genetic predisposition to disease
Genetic testing
Genetic variation
Inheritance patterns
Risk factors
Penetrence
title_short Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variants
title_full Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variants
title_fullStr Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variants
title_full_unstemmed Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variants
title_sort Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variants
dc.creator.none.fl_str_mv García Hernandez, Soledad
De la Higuera Romero, Luis
Fernandez, Adrian
Luisa Peña Peña, Maria
Mora Ayestaran, Nerea
Basurte Elorz, María Teresa
Larrañaga Moreira, Jose María
Cárdenas Reyes, Ivonne
Villacorta, Eduardo
Valverde Gómez, Maria
Baustista-Paves, Alicia
Veira Villanueva, Elena
Ortiz Genga, Martín
Lipov, Alex
Brogger, Noel
Sabater Molina, María
Moreno Escobar, Eduardo
Ruiz Guerrero, Luis Javier
Syrris, Petros
Piqueras Flores, Jesús
author García Hernandez, Soledad
author_facet García Hernandez, Soledad
De la Higuera Romero, Luis
Fernandez, Adrian
Luisa Peña Peña, Maria
Mora Ayestaran, Nerea
Basurte Elorz, María Teresa
Larrañaga Moreira, Jose María
Cárdenas Reyes, Ivonne
Villacorta, Eduardo
Valverde Gómez, Maria
Baustista-Paves, Alicia
Veira Villanueva, Elena
Ortiz Genga, Martín
Lipov, Alex
Brogger, Noel
Sabater Molina, María
Moreno Escobar, Eduardo
Ruiz Guerrero, Luis Javier
Syrris, Petros
Piqueras Flores, Jesús
author_role author
author2 De la Higuera Romero, Luis
Fernandez, Adrian
Luisa Peña Peña, Maria
Mora Ayestaran, Nerea
Basurte Elorz, María Teresa
Larrañaga Moreira, Jose María
Cárdenas Reyes, Ivonne
Villacorta, Eduardo
Valverde Gómez, Maria
Baustista-Paves, Alicia
Veira Villanueva, Elena
Ortiz Genga, Martín
Lipov, Alex
Brogger, Noel
Sabater Molina, María
Moreno Escobar, Eduardo
Ruiz Guerrero, Luis Javier
Syrris, Petros
Piqueras Flores, Jesús
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidad de Cantabria
dc.subject.none.fl_str_mv Cardiomyopathy
Hypertrophic
Genetic predisposition to disease
Genetic testing
Genetic variation
Inheritance patterns
Risk factors
Penetrence
topic Cardiomyopathy
Hypertrophic
Genetic predisposition to disease
Genetic testing
Genetic variation
Inheritance patterns
Risk factors
Penetrence
description Background: Hypertrophic cardiomyopathy (HCM) is a genetically heterogeneous disorder linked primarily to rare variants in sarcomeric genes, although recently certain nonsarcomeric genes have emerged as important contributors. Nonmendelian genetic variants with reproducible moderate-effect sizes and low penetrance, intermediate-effect variants (IEVs), can play a crucial role in modulating disease expression. Understanding the clinical impact of IEVs is crucial to unravel the complex genetic architecture of HCM. Methods: We conducted an ancestry-based enrichment analysis of 14 validated HCM genes, including the 9 core sarcomeric and 5 nonsarcomeric genes (ALPK3, CSRP3, FHOD3, FLNC, and TRIM63). Enrichment of intermediate frequency missense variants was evaluated in 10 981 patients with HCM, 4030 internal controls of European-ancestry, and 590 000 external controls from gnomAD non-Finnish Europeans. The population-attributable fraction was calculated to assess contribution of IEVs to HCM. Age-related disease penetrance, phenotypic severity (left ventricular maximum wall thickness), and major adverse cardiac events were analyzed in 11 991 HCM cases of the whole cohort according to 5 genetic groups: genotype negative, isolated IEV, monogenic, monogenic+IEV, and double monogenic. Results: Fourteen IEVs in 8 genes were identified in 731 individuals (6.1% of the cohort), of whom 570 patients (4.8%) had IEVs in isolation: 198 (34.7%) in sarcomeric genes and 372 (65.3%) in nonsarcomeric genes. The contribution of IEVs to HCM genetics according to population-attributable fraction was estimated to be 4.9% (95% CI, 3.2-6.7). A significant gradient in penetrance, phenotypic severity, and major adverse cardiac events was observed across genetic groups. Compared with genotype-negative patients, IEV carriers displayed a younger median age at diagnosis (59 years of age [95% CI, 46-69] versus 61 years [95% CI, 49-70]; P=0.0073) and a higher mean left ventricular maximum wall thickness (18.1±3.7 versus 19.0±4.3; P=0.0043). IEVs also modified disease expression in individuals with monogenic variants, causing a more aggressive phenotype than in individuals from the monogenic-only group with HCM onset at younger age and a higher left ventricular maximum wall thickness (all P<0.0001), with major adverse cardiac event-free survival being significantly lower (93.3% versus 69.3% at 70 years of age; P<0.0001). Conclusions: IEVs are present in 6.1% of HCM cases and account for 4.8% of HCM genetic burden. IEVs also influence disease severity and outcomes, particularly when combined with monogenic disease-causing variants. Evaluation of IEVs should be considered when HCM genetic testing is performed.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025-01-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
NA
http://purl.org/coar/version/c_be7fb7dd8ff6fe43
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/10902/38807
url https://hdl.handle.net/10902/38807
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial-NoDerivatives 4.0 International
http://creativecommons.org/licenses/by-nc-nd/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial-NoDerivatives 4.0 International
http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv American Heart Association
publisher.none.fl_str_mv American Heart Association
dc.source.none.fl_str_mv Circulation, 2025, 152(15), 1060-1075
reponame:UCrea Repositorio Abierto de la Universidad de Cantabria
instname:Universidad de Cantabria (UC)
instname_str Universidad de Cantabria (UC)
reponame_str UCrea Repositorio Abierto de la Universidad de Cantabria
collection UCrea Repositorio Abierto de la Universidad de Cantabria
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869421580785811456
spelling Redefining the genetic architecture of hypertrophic cardiomyopathy: role of intermediate-effect variantsGarcía Hernandez, SoledadDe la Higuera Romero, LuisFernandez, AdrianLuisa Peña Peña, MariaMora Ayestaran, NereaBasurte Elorz, María TeresaLarrañaga Moreira, Jose MaríaCárdenas Reyes, IvonneVillacorta, EduardoValverde Gómez, MariaBaustista-Paves, AliciaVeira Villanueva, ElenaOrtiz Genga, MartínLipov, AlexBrogger, NoelSabater Molina, MaríaMoreno Escobar, EduardoRuiz Guerrero, Luis JavierSyrris, PetrosPiqueras Flores, JesúsCardiomyopathyHypertrophicGenetic predisposition to diseaseGenetic testingGenetic variationInheritance patternsRisk factorsPenetrenceBackground: Hypertrophic cardiomyopathy (HCM) is a genetically heterogeneous disorder linked primarily to rare variants in sarcomeric genes, although recently certain nonsarcomeric genes have emerged as important contributors. Nonmendelian genetic variants with reproducible moderate-effect sizes and low penetrance, intermediate-effect variants (IEVs), can play a crucial role in modulating disease expression. Understanding the clinical impact of IEVs is crucial to unravel the complex genetic architecture of HCM. Methods: We conducted an ancestry-based enrichment analysis of 14 validated HCM genes, including the 9 core sarcomeric and 5 nonsarcomeric genes (ALPK3, CSRP3, FHOD3, FLNC, and TRIM63). Enrichment of intermediate frequency missense variants was evaluated in 10 981 patients with HCM, 4030 internal controls of European-ancestry, and 590 000 external controls from gnomAD non-Finnish Europeans. The population-attributable fraction was calculated to assess contribution of IEVs to HCM. Age-related disease penetrance, phenotypic severity (left ventricular maximum wall thickness), and major adverse cardiac events were analyzed in 11 991 HCM cases of the whole cohort according to 5 genetic groups: genotype negative, isolated IEV, monogenic, monogenic+IEV, and double monogenic. Results: Fourteen IEVs in 8 genes were identified in 731 individuals (6.1% of the cohort), of whom 570 patients (4.8%) had IEVs in isolation: 198 (34.7%) in sarcomeric genes and 372 (65.3%) in nonsarcomeric genes. The contribution of IEVs to HCM genetics according to population-attributable fraction was estimated to be 4.9% (95% CI, 3.2-6.7). A significant gradient in penetrance, phenotypic severity, and major adverse cardiac events was observed across genetic groups. Compared with genotype-negative patients, IEV carriers displayed a younger median age at diagnosis (59 years of age [95% CI, 46-69] versus 61 years [95% CI, 49-70]; P=0.0073) and a higher mean left ventricular maximum wall thickness (18.1±3.7 versus 19.0±4.3; P=0.0043). IEVs also modified disease expression in individuals with monogenic variants, causing a more aggressive phenotype than in individuals from the monogenic-only group with HCM onset at younger age and a higher left ventricular maximum wall thickness (all P<0.0001), with major adverse cardiac event-free survival being significantly lower (93.3% versus 69.3% at 70 years of age; P<0.0001). Conclusions: IEVs are present in 6.1% of HCM cases and account for 4.8% of HCM genetic burden. IEVs also influence disease severity and outcomes, particularly when combined with monogenic disease-causing variants. Evaluation of IEVs should be considered when HCM genetic testing is performed.This project was funded by Bristol-Myers Squibb. Drs Bezzina and García-Pavía are supported by the Pathfinder Cardiogenomics program of the European Innovation Council of the European Union (DCM-NEXT project).American Heart AssociationUniversidad de Cantabria20252025-01-01journal articlehttp://purl.org/coar/resource_type/c_6501NAhttp://purl.org/coar/version/c_be7fb7dd8ff6fe43info:eu-repo/semantics/articlehttps://hdl.handle.net/10902/38807Circulation, 2025, 152(15), 1060-1075reponame:UCrea Repositorio Abierto de la Universidad de Cantabriainstname:Universidad de Cantabria (UC)Inglésengopen accesshttp://purl.org/coar/access_right/c_abf2Attribution-NonCommercial-NoDerivatives 4.0 Internationalhttp://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:repositorio.unican.es:10902/388072026-06-02T12:39:31Z
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