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1. Analysis of age-related left ventricular collagen remodeling in living donors: Implications in arrhythmogenesis

Author

Laura García-Mendívil, María Pérez-Zabalza, Konstantinos Mountris, Sam Duwé, Nick Smisdom, Marta Pérez, Lluís Luján, Esther Wolfs, Ronald B. Driesen, José María Vallejo-Gil, Pedro Carlos Fresneda-Roldán, Javier Fañanás-Mastral, Manuel Vázquez-Sancho, Marta Matamala-Adell, Juan Fernando Sorribas-Berjón, Javier André Bellido-Morales, Francisco Javier Mancebón-Sierra, Alexánder Sebastián Vaca-Núñez, Carlos Ballester-Cuenca, Aida Oliván-Viguera, Emiliano Diez, Laura Ordovás, and Esther Pueyo

Subjects
Disease, Pathophysiology, Computational bioinformatics, Science
Abstract

Summary: Age-related fibrosis in the left ventricle (LV) has been mainly studied in animals by assessing collagen content. Using second-harmonic generation microscopy and image processing, we evaluated amount, aggregation and spatial distribution of LV collagen in young to old pigs, and middle-age and elder living donors. All collagen features increased when comparing adult and old pigs with young ones, but not when comparing adult with old pigs or middle-age with elder individuals. Remarkably, all collagen parameters strongly correlated with lipofuscin, a biological age marker, in humans. By building patient-specific models of human ventricular tissue electrophysiology, we confirmed that amount and organization of fibrosis modulated arrhythmia vulnerability, and that distribution should be accounted for arrhythmia risk assessment. In conclusion, we characterize the age-associated changes in LV collagen and its potential implications for ventricular arrhythmia development. Consistency between pig and human results substantiate the pig as a relevant model of age-related LV collagen dynamics.

Published
2022
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2. Automatic Quantification of Cardiomyocyte Dimensions and Connexin 43 Lateralization in Fluorescence Images

Author

Antoni Oliver-Gelabert, Laura García-Mendívil, José María Vallejo-Gil, Pedro Carlos Fresneda-Roldán, Katarína Andelová, Javier Fañanás-Mastral, Manuel Vázquez-Sancho, Marta Matamala-Adell, Fernando Sorribas-Berjón, Carlos Ballester-Cuenca, Narcisa Tribulova, Laura Ordovás, Emiliano Raúl Diez, and Esther Pueyo

Subjects
automated quantification, Connexin 43, fluorescent microscopy, lateralization, cardiomyocytes, Microbiology, QR1-502
Abstract

Cardiomyocytes’ geometry and connexin 43 (CX43) amount and distribution are structural features that play a pivotal role in electrical conduction. Their quantitative assessment is of high interest in the study of arrhythmias, but it is usually hampered by the lack of automatic tools. In this work, we propose a software algorithm (Myocyte Automatic Retrieval and Tissue Analyzer, MARTA) to automatically detect myocytes from fluorescent microscopy images of cardiac tissue, measure their morphological features and evaluate the expression of CX43 and its degree of lateralization. The proposed software is based on the generation of cell masks, contouring of individual cells, enclosing of cells in minimum area rectangles and splitting of these rectangles into end-to-end and middle compartments to estimate CX43 lateral-to-total ratio. Application to human ventricular tissue images shows that mean differences between automatic and manual methods in terms of cardiomyocyte length and width are below 4 μm. The percentage of lateral CX43 also agrees between automatic and manual evaluation, with the interquartile range approximately covering from 3% to 30% in both cases. MARTA is not limited by fiber orientation and has an optimized speed by using contour filtering, which makes it run hundreds of times faster than a trained expert. Developed for CX43 studies in the left ventricle, MARTA is a flexible tool applicable to morphometric and lateralization studies of other markers in any heart chamber or even skeletal muscle. This open-access software is available online.

Published
2020
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3. Minimally invasive system to reliably characterize ventricular electrophysiology from living donors

Author

Carlos Ballester-Cuenca, Laura García-Mendívil, José María Vallejo-Gil, Francisco Javier Mancebón-Sierra, Emiliano Raúl Diez, Fernando Sorribas-Berjón, Miguel Angel Marigil, Sofía Orós-Rodrigo, Estel Ramos-Marquès, Manuel Vázquez-Sancho, Maria Perez-Zabalza, Javier André Bellido-Morales, Alexánder Sebastián Vaca-Núñez, Konstantinos A. Mountris, Aida Oliván-Viguera, Ralf Köhler, Laura Ordovás, Javier Fañanás-Mastral, Pedro Carlos Fresneda-Roldán, Cristina Pastor, Esther Pueyo, and Marta Matamala-Adell

Subjects
0301 basic medicine, Cell biology, Tissue architecture, Pathology, medicine.medical_specialty, Molecular biology, Swine, Heart Ventricles, Cardiology, lcsh:Medicine, Action Potentials, 030204 cardiovascular system & hematology, MYOCARDIAL SLICE, Article, Membrane Potentials, 03 medical and health sciences, 0302 clinical medicine, LIVING DONORS, Living Donors, Animals, Humans, Medicine, Cellular organization, lcsh:Science, Multidisciplinary, business.industry, lcsh:R, ACTION POTENTIALS, purl.org/becyt/ford/3.1 [https], ELECTROPHYSIOLOGY, Electrophysiological Phenomena, 3. Good health, Electrophysiology, 030104 developmental biology, Vital stain, Action potential duration, lcsh:Q, purl.org/becyt/ford/3 [https], Cardiac Electrophysiology, business, Core biopsy
Abstract

Cardiac tissue slices preserve the heterogeneous structure and multicellularity of the myocardium and allow its functional characterization. However, access to human ventricular samples is scarce. We aim to demonstrate that slices from small transmural core biopsies collected from living donors during routine cardiac surgery preserve structural and functional properties of larger myocardial specimens, allowing accurate electrophysiological characterization. In pigs, we compared left ventricular transmural core biopsies with transmural tissue blocks from the same ventricular region. In humans, we analyzed transmural biopsies and papillary muscles from living donors. All tissues were vibratomesliced. By histological analysis of the transmural biopsies, we showed that tissue architecture and cellular organization were preserved. Enzymatic and vital staining methods verifed viability. Optically mapped transmembrane potentials confrmed that action potential duration and morphology were similar in pig biopsies and tissue blocks. Action potential morphology and duration in human biopsies and papillary muscles agreed with published ranges. In both pigs and humans, responses to increasing pacing frequencies and β-adrenergic stimulation were similar in transmural biopsies and larger tissues. We show that it is possible to successfully collect and characterize tissue slices from human myocardial biopsies routinely extracted from living donors, whose behavior mimics that of larger myocardial preparations both structurally and electrophysiologically. Fil: Oliván Viguera, Aida. Universidad de Zaragoza; España Fil: Pérez Zabalza, María. Universidad de Zaragoza; España Fil: García Mendívil, Laura. Universidad de Zaragoza; España Fil: Mountris, Konstantinos A.. Universidad de Zaragoza; España Fil: Orós Rodrigo, Sofía. Universidad de Zaragoza; España Fil: Ramos Marquès, Estel. Universidad de Zaragoza; España Fil: Vallejo Gil, José María. University Hospital Miguel Servet; España Fil: Fresneda Roldán, Pedro Carlos. University Hospital Miguel Servet; España Fil: Fañanás Mastral, Javier. University Hospital Miguel Servet; España Fil: Vázquez Sancho, Manuel. University Hospital Miguel Servet; España Fil: Matamala Adell, Marta. University Hospital Miguel Servet; España Fil: Sorribas Berjón, Fernando. University Hospital Miguel Servet; España Fil: Bellido Morales, Javier André. University Hospital Miguel Servet; España Fil: Mancebón Sierra, Francisco Javier. University Hospital Miguel Servet; España Fil: Vaca Núñez, Alexánder Sebastián. University Hospital Miguel Servet; España Fil: Ballester Cuenca, Carlos. University Hospital Miguel Servet; España Fil: Marigil, Miguel Ángel. Hospital San Jorge; España Fil: Pastor, Cristina. Aragón Institute of Health Sciences; España Fil: Ordovás, Laura. Aragón Agency for Research and Development; España. Universidad de Zaragoza; España Fil: Köhler, Ralf. Aragón Institute of Health Sciences; España. Aragón Agency for Research and Development; España Fil: Diez, Emiliano Raúl. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas. Cátedra de Fisiología Humana Normal; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Medicina y Biología Experimental de Cuyo; Argentina Fil: Pueyo, Esther. Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina; España. Universidad de Zaragoza; España

Published
2020

4. Automatic Quantification of Cardiomyocyte Dimensions and Connexin 43 Lateralization in Fluorescence Images

Author

Katarina Andelova, Manuel Vázquez-Sancho, Emiliano Raúl Diez, Narcisa Tribulova, Laura García-Mendívil, José María Vallejo-Gil, Carlos Ballester-Cuenca, Laura Ordovás, Pedro Carlos Fresneda-Roldán, Antoni Oliver-Gelabert, Esther Pueyo, Marta Matamala-Adell, Fernando Sorribas-Berjón, and Javier Fañanás-Mastral

Subjects
0301 basic medicine, Male, Spectrum analyzer, AUTOMATED QUANTIFICATION, Computer science, LATERALIZATION, Heart chamber, lcsh:QR1-502, Connexin, cardiomyocytes, 030204 cardiovascular system & hematology, Biochemistry, Lateralization of brain function, Article, lcsh:Microbiology, CARDIOMYOCYTES, Sarcoplasmic Reticulum Calcium-Transporting ATPases, 03 medical and health sciences, 0302 clinical medicine, Software, medicine, Myocyte, Animals, Humans, lateralization, Myocytes, Cardiac, Rats, Wistar, Molecular Biology, Contouring, CONNEXIN 43, business.industry, Myocardium, purl.org/becyt/ford/3.1 [https], 030104 developmental biology, medicine.anatomical_structure, FLUORESCENT MICROSCOPY, Microscopy, Fluorescence, Ventricle, Connexin 43, cardiovascular system, purl.org/becyt/ford/3 [https], business, automated quantification, Algorithms, Biomedical engineering, fluorescent microscopy
Abstract

Cardiomyocytes&rsquo, geometry and connexin 43 (CX43) amount and distribution are structural features that play a pivotal role in electrical conduction. Their quantitative assessment is of high interest in the study of arrhythmias, but it is usually hampered by the lack of automatic tools. In this work, we propose a software algorithm (Myocyte Automatic Retrieval and Tissue Analyzer, MARTA) to automatically detect myocytes from fluorescent microscopy images of cardiac tissue, measure their morphological features and evaluate the expression of CX43 and its degree of lateralization. The proposed software is based on the generation of cell masks, contouring of individual cells, enclosing of cells in minimum area rectangles and splitting of these rectangles into end-to-end and middle compartments to estimate CX43 lateral-to-total ratio. Application to human ventricular tissue images shows that mean differences between automatic and manual methods in terms of cardiomyocyte length and width are below 4 &mu, m. The percentage of lateral CX43 also agrees between automatic and manual evaluation, with the interquartile range approximately covering from 3% to 30% in both cases. MARTA is not limited by fiber orientation and has an optimized speed by using contour filtering, which makes it run hundreds of times faster than a trained expert. Developed for CX43 studies in the left ventricle, MARTA is a flexible tool applicable to morphometric and lateralization studies of other markers in any heart chamber or even skeletal muscle. This open-access software is available online.

Published
2020
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5. Chronological and biological aging of the human left ventricular myocardium: Analysis of microRNAs contribution

Author

Estel Ramos-Marquès, Elisa Garrido-Huéscar, Juan Carlos Oliveros, Javier André Bellido-Morales, Carlos Ballester-Cuenca, José María Vallejo-Gil, Francisco Javier Mancebón-Sierra, Gorka Muñiz, Javier Fañanás-Mastral, Aida Oliván-Viguera, Manuel F. Jiménez-Navarro, Carlos Gómez-González, Juan Fernando Sorribas-Berjón, Margarita Segovia-Roldan, Hazel Santander-Badules, Alberto Cebollada, Laura García-Mendívil, Maria Perez-Zabalza, Alexánder Sebastián Vaca-Núñez, Jose M. Villaescusa, Esther Pueyo, Marta Matamala-Adell, Laura Ordovás, Emiliano Raúl Diez, Manuel Vázquez-Sancho, Sabarathinam Srinivasan, Pedro Carlos Fresneda-Roldán, Rafael Torres-Pérez, [Ramos-Marquès,E, García-Mendívil,L, Pérez-Zabalza,M, Santander-Badules,H, Srinivasan,S, Garrido-Huéscar,E, Segovia-Roldán,M, Oliván-Viguera,A, Ordovás,L, Pueyo,E] Biomedical Signal Interpretation and Computational Simulation group (BSICoS), Aragón Institute of Engineering Research, University of Zaragoza, Zaragoza, Spain. [Ramos-Marquès,E, Pueyo,E] BSICoS, IIS Aragón, Zaragoza, Spain. [Oliveros,JC, Torres-Pérez,R] Bioinformatics for Genomics and Proteomics, National Center of Biotechnology- Spanish National Research Council, Madrid, Spain. [Cebollada,A] Biocomputation unit, IACS, Zaragoza, Spain. [Vallejo-Gil,JM, Fresneda-Roldán,PC, Fañanás-Mastral,J, Vázquez-Sancho,M, Matamala-Adell,M, Sorribas-Berjón,JF, Bellido-Morales,JA, Mancebón-Sierra,FJ, Vaca-Núñez,AS, Ballester-Cuenca,C] Department of Cardiovascular Surgery, University Hospital Miguel Servet, Zaragoza, Spain. [Jiménez-Navarro,M] Heart Area, Hospital Clínico Universitario Virgen de la Victoria, CIBERCV, IBIMA, Universidad de Málaga, UMA, Málaga, Spain. [Villaescusa,JM] UGC Heart Area, Cardiovascular Surgery Department, Hospital Universitario Virgen de la Victoria de Málaga, Fundación Pública Andaluza para la Investigación de Málaga en Biomedicina y Salud (FIMABIS), CIBERCV Enfermedades Cardiovasculares, Instituto de Salud Carlos III, University of Málaga, Madrid, Spain. [Gómez-González,C, Muñiz,G] Department of Pathology, San Jorge Hospital, Huesca, Spain. [Diez,E] Institute of Experimental Medicine and Biology of Cuyo (IMBECU), CONICET, Mendoza, Argentina. [Ordovás,L] ARAID Foundation, Zaragoza, Spain. [Pueyo,E] Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Zaragoza, Spain, and The Genotype-Tissue Expression (GTEx) Project was supported by the Common Fund of the Office of the Director of the National Institutes of Health, and by NCI, NHGRI, NHLBI, NIDA, NIMH, and NINDS.

Subjects
0301 basic medicine, Male, Aging, Phenomena and Processes::Genetic Phenomena::Phenotype [Medical Subject Headings], Cardiac fibrosis, Envejecimiento, Persons::Persons::Tissue Donors::Living Donors [Medical Subject Headings], Bioinformatics, Analytical, Diagnostic and Therapeutic Techniques and Equipment::Investigative Techniques::Epidemiologic Methods::Statistics as Topic::Probability::Risk::Risk Factors [Medical Subject Headings], Transcriptome, Organisms::Eukaryota::Animals::Chordata::Vertebrates::Mammals::Primates::Haplorhini::Catarrhini::Hominidae::Humans [Medical Subject Headings], 0302 clinical medicine, CDKN2A, Ventrículos cardíacos, Heart ventricles, Donadores vivos, MicroARNs, microRNA, transcriptomic age marker, Phenotype, Anatomy::Cardiovascular System::Heart::Heart Ventricles [Medical Subject Headings], 3. Good health, medicine.anatomical_structure, Heart aging, Disciplines and Occupations::Natural Science Disciplines::Biological Science Disciplines::Biology::Computational Biology [Medical Subject Headings], biological aging, Biomarker (medicine), Female, Redes reguladoras de genes, Senescence, gene regulation network, Heart Ventricles, Check Tags::Male [Medical Subject Headings], Phenomena and Processes::Genetic Phenomena::Genetic Structures::Base Sequence::Regulatory Sequences, Nucleic Acid::Gene Regulatory Networks [Medical Subject Headings], Biology, Phenomena and Processes::Chemical Phenomena::Biochemical Phenomena::Biochemical Processes::Transcription, Genetic::Transcriptome [Medical Subject Headings], 03 medical and health sciences, Biological aging, Phenomena and Processes::Physiological Phenomena::Physiological Processes::Growth and Development::Aging [Medical Subject Headings], medicine, Humans, Living donors, Gene regulation network, Original Paper, Myocardium, biomarkers, Cell Biology, Original Articles, Anatomy::Cardiovascular System::Heart::Myocardium [Medical Subject Headings], medicine.disease, Transcriptoma, Chemicals and Drugs::Nucleic Acids, Nucleotides, and Nucleosides::Antisense Elements (Genetics)::RNA, Antisense::MicroRNAs [Medical Subject Headings], MicroRNAs, 030104 developmental biology, Biomarcadores, Miocardio, Check Tags::Female [Medical Subject Headings], Ventricle, heart aging, Transcriptomic age marker, 030217 neurology & neurosurgery, Biomarkers
Abstract

Aging is the main risk factor for cardiovascular diseases. In humans, cardiac aging remains poorly characterized. Most studies are based on chronological age (CA) and disregard biological age (BA), the actual physiological age (result of the aging rate on the organ structure and function), thus yielding potentially imperfect outcomes. Deciphering the molecular basis of ventricular aging, especially by BA, could lead to major progresses in cardiac research. We aim to describe the transcriptome dynamics of the aging left ventricle (LV) in humans according to both CA and BA and characterize the contribution of microRNAs, key transcriptional regulators. BA is measured using two CA‐associated transcriptional markers: CDKN2A expression, a cell senescence marker, and apparent age (AppAge), a highly complex transcriptional index. Bioinformatics analysis of 132 LV samples shows that CDKN2A expression and AppAge represent transcriptomic changes better than CA. Both BA markers are biologically validated in relation to an aging phenotype associated with heart dysfunction, the amount of cardiac fibrosis. BA‐based analyses uncover depleted cardiac‐specific processes, among other relevant functions, that are undetected by CA. Twenty BA‐related microRNAs are identified, and two of them highly heart‐enriched that are present in plasma. We describe a microRNA‐gene regulatory network related to cardiac processes that are partially validated in vitro and in LV samples from living donors. We prove the higher sensitivity of BA over CA to explain transcriptomic changes in the aging myocardium and report novel molecular insights into human LV biological aging. Our results can find application in future therapeutic and biomarker research., The biological age, measured by transcriptional markers, explains better than the chronological age the transcriptional dynamics of the human aging myocardium. microRNAs that change expression in the aging left ventricle are identified. Such microRNAs potentially regulate genes with cardiac‐specific functions. Cardiac‐enriched microRNAs that increase or decrease with biological age are present in plasma. They are thus candidate biomarkers to represent the biological age of the heart.

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6. Improved Methods for Processing Optical Mapping Signals From Human Left Ventricular Tissues at Baseline and Following Adrenergic Stimulation

Author

Carlos Ballester-Cuenca, Esther Pueyo, Marta Matamala-Adell, Emiliano Raúl Diez, Aida Oliván-Viguera, Margarita Segovia-Roldan, Maria Perez-Zabalza, José María Vallejo-Gil, Kostantinos A Mountris, Fernando Sorribas-Berjón, Pedro Carlos Fresneda-Roldán, Manuel Vázquez-Sancho, Julia Rhyins, and Javier Fañanás-Mastral

Subjects
0301 basic medicine, Signal processing, Noise measurement, Noise (signal processing), Computer science, HUMAN VENTRICULAR ELECTROPHYSIOLOGY, purl.org/becyt/ford/1.2 [https], White noise, Avalanche photodiode, purl.org/becyt/ford/1 [https], 03 medical and health sciences, Electrophysiology, 030104 developmental biology, 0302 clinical medicine, OPTICAL MAPPING, DRIFT REMOVAL, Optical mapping, SIGNAL PROCESSING, OMAP, 030217 neurology & neurosurgery, Biomedical engineering
Abstract

Optical mapping (OM) allows ex vivo measurement of electrophysiological signals at high spatio-temporal resolution, but the signal-to-roise ratio is commonly low. A variety of software options have been proposed to extract relevant information from OM recordings, being ElectroMap the most advanced tool currently available. In this study, improved methods are presented for processing OM signals of cardiac transmembrane voltage. A software called OMap is developed that incorporates novel techniques into ElectroMap for improved baseline drift removal, spatiotemporal filtering and characterization of action potential duration (APD) maps. In synthetically generated signals contaminated with baseline wander, white noise and the combination of both, the errors in APD maps between noisy and clean signals are remarkably lower for OMap than for ElectroMap, particularly for high noise levels. In OM signals recorded from human ventricular tissue specimens, OMap allows to clearly characterize the APD shortening effect induced by ß-adrenergic stimulation, whereas ElectroMap renders highly overlapped APD distributions for baseline and ß-adrenergic stimulation. In conclusion, improved methods are proposed and tested to characterize human ventricular electrophysiology from noisy OM recordings. Fil: Perez Zabalza, Maria. Universidad de Zaragoza; España Fil: Diez, Emiliano Raúl. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto de Medicina y Biología Experimental de Cuyo; Argentina Fil: Rhyins, Julia. Northeastern University; Estados Unidos Fil: Mountris, Kostantinos A.. Universidad de Zaragoza; España Fil: Vallejo Gil, Jose M.. Hospital Miguel Servet; España Fil: Fresneda Roldan, Pedro C.. Hospital Miguel Servet; España Fil: Fananas-Mastral, Javier. Hospital Miguel Servet; España Fil: Matamal Adell, Marta. Hospital Miguel Servet; España Fil: Sorribas Berjon, Fernando. Hospital Miguel Servet; España Fil: Vazquez Sancho, Manuel. Hospital Miguel Servet; España Fil: Ballester Cuenca, Carlos. Hospital Miguel Servet; España Fil: Segovia Roldan, Margarita. Universidad de Zaragoza; España Fil: Olivan Viguera, Aida. Universidad de Zaragoza; España Fil: Pueyo, Esther. Universidad de Zaragoza; España

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