{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T20:00:32Z","timestamp":1790193632328,"version":"4.1.0"},"reference-count":91,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2025,5,19]],"date-time":"2025-05-19T00:00:00Z","timestamp":1747612800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000968","name":"American Heart Association","doi-asserted-by":"publisher","award":["899419"],"award-info":[{"award-number":["899419"]}],"id":[{"id":"10.13039\/100000968","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005562","name":"North Carolina Biotechnology Center","doi-asserted-by":"publisher","award":["2016-IDG-1016"],"award-info":[{"award-number":["2016-IDG-1016"]}],"id":[{"id":"10.13039\/100005562","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008615","name":"Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill","doi-asserted-by":"publisher","award":["P30 CA016086"],"award-info":[{"award-number":["P30 CA016086"]}],"id":[{"id":"10.13039\/100008615","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100017540","name":"NHLBI Division of Intramural Research","doi-asserted-by":"publisher","award":["R01HL146626"],"award-info":[{"award-number":["R01HL146626"]}],"id":[{"id":"10.13039\/100017540","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>Congenital heart defects occur in approximately 1% of newborns in the US annually. Currently, less than a third of congenital heart defects can be traced to a known genetic or environmental cause, suggesting that a large proportion of disease-causing mechanisms have yet to be fully characterized. Hemodynamic forces such as wall shear stress are critical for heart development and are known to induce changes in embryonic cardiac patterning leading to malformations. However, measuring these hemodynamic factors <jats:italic>in vivo<\/jats:italic> is infeasible due to physical limitations, such as the small size and constant motion of the embryonic heart. This serves as a significant barrier towards developing a mechanics-based understanding of the origins of congenital heart defects. An alternative approach is to recapitulate the hemodynamic environment by simulating blood flow and calculating the resulting hemodynamic forces through computational fluid dynamics modeling. Thus, we have developed a robust computational fluid dynamics modeling pipeline to quantify hemodynamics within cell-accurate anatomies of embryonic chick hearts. Here we describe the implementation of single plane illumination light sheet fluorescent microscopy to generate full three-dimensional reconstructions of the embryonic heart <jats:italic>in silico<\/jats:italic>, quantitative geometric morphometric methods for identifying anatomic variability across samples, and computational fluid dynamic approaches for calculating flow, pressure, and wall shear stress within complex tissue architectures. Together, these methods produce a fast, robust, and accessible system of analysis for generating high-resolution, quantitative descriptions of anatomical variability and hemodynamic forces in the embryonic heart.<\/jats:p>","DOI":"10.1371\/journal.pone.0322233","type":"journal-article","created":{"date-parts":[[2025,5,19]],"date-time":"2025-05-19T17:50:55Z","timestamp":1747677055000},"page":"e0322233","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["An anatomically informed computational fluid dynamics modeling approach for quantifying hemodynamics in the developing heart"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5796-4212","authenticated-orcid":true,"given":"Kirsten","family":"Giesbrecht","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simone","family":"Rossi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sophie","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shourya","family":"Mukherjee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5200-931X","authenticated-orcid":true,"given":"Michael","family":"Bressan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9800-7504","authenticated-orcid":true,"given":"Boyce E.","family":"Griffith","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,5,19]]},"reference":[{"issue":"8","key":"pone.0322233.ref001","article-title":"Heart Disease and Stroke Statistics-2022 Update: A Report From the American Heart Association","volume":"145","author":"CW Tsao","year":"2022","journal-title":"Circulation"},{"issue":"12","key":"pone.0322233.ref002","doi-asserted-by":"crossref","first-page":"1890","DOI":"10.1016\/S0735-1097(02)01886-7","article-title":"The incidence of congenital heart disease","volume":"39","author":"JIE Hoffman","year":"2002","journal-title":"J Am Coll Cardiol"},{"issue":"2","key":"pone.0322233.ref003","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/S0167-5273(98)00354-4","article-title":"Syndromes and malformations associated with congenital heart disease in a population-based study","volume":"68","author":"V Grech","year":"1999","journal-title":"Int J Cardiol"},{"issue":"8","key":"pone.0322233.ref004","doi-asserted-by":"crossref","first-page":"1142","DOI":"10.1111\/j.1651-2227.2007.00381.x","article-title":"Congenital heart defects--chromosomal anomalies, syndromes and extracardiac malformations","volume":"96","author":"A Meberg","year":"2007","journal-title":"Acta Paediatr"},{"issue":"11","key":"pone.0322233.ref005","doi-asserted-by":"crossref","first-page":"827","DOI":"10.3390\/medicina44110104","article-title":"Selected environmental risk factors and congenital heart defects","volume":"44","author":"R Kuciene","year":"2008","journal-title":"Medicina (Kaunas)"},{"key":"pone.0322233.ref006","doi-asserted-by":"crossref","first-page":"287","DOI":"10.3389\/fphys.2014.00287","article-title":"Congenital heart malformations induced by hemodynamic altering surgical interventions","volume":"5","author":"M Midgett","year":"2014","journal-title":"Front Physiol"},{"issue":"2","key":"pone.0322233.ref007","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1007\/s10237-020-01413-5","article-title":"Effect of left atrial ligation-driven altered inflow hemodynamics on embryonic heart development: clues for prenatal progression of hypoplastic left heart syndrome","volume":"20","author":"HE Salman","year":"2021","journal-title":"Biomech Model Mechanobiol"},{"issue":"4","key":"pone.0322233.ref008","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1161\/01.RES.80.4.473","article-title":"Unilateral vitelline vein ligation alters intracardiac blood flow patterns and morphogenesis in the chick embryo","volume":"80","author":"B Hogers","year":"1997","journal-title":"Circ Res"},{"key":"pone.0322233.ref009","doi-asserted-by":"crossref","first-page":"849603","DOI":"10.3389\/fphys.2022.849603","article-title":"Blood Flow Disturbance and Morphological Alterations Following the Right Atrial Ligation in the Chick Embryo","volume":"13","author":"M Alser","year":"2022","journal-title":"Front Physiol"},{"key":"pone.0322233.ref010","article-title":"Shear and hydrostatic stress regulate fetal heart valve remodeling through YAP-mediated mechanotransduction","volume":"12","author":"M Wang","year":"2023","journal-title":"Elife"},{"issue":"2","key":"pone.0322233.ref011","first-page":"23","article-title":"Validating the Paradigm That Biomechanical Forces Regulate Embryonic Cardiovascular Morphogenesis and Are Fundamental in the Etiology of Congenital Heart Disease","volume":"7","author":"BB Keller","year":"2020","journal-title":"J Cardiovasc Dev Dis"},{"key":"pone.0322233.ref012","first-page":"380","article-title":"The role of shear stress on ET-1, KLF2, and NOS-3 expression in the developing cardiovascular system of chicken embryos in a venous ligation model","volume":"22","author":"BCW Groenendijk","year":"2007","journal-title":"Physiology (Bethesda)"},{"issue":"1","key":"pone.0322233.ref013","article-title":"Characterization of the vessel geometry, flow mechanics and wall shear stress in the great arteries of wildtype prenatal mouse","volume":"9","author":"CH Yap","year":"2014","journal-title":"PLoS One"},{"issue":"2","key":"pone.0322233.ref014","first-page":"108","article-title":"Altered Hemodynamics in the Embryonic Heart Affects Outflow Valve Development","volume":"2","author":"V Menon","year":"2015","journal-title":"J Cardiovasc Dev Dis"},{"issue":"20","key":"pone.0322233.ref015","doi-asserted-by":"crossref","DOI":"10.1242\/dev.162578","article-title":"Cohort-based multiscale analysis of hemodynamic-driven growth and remodeling of the embryonic pharyngeal arch arteries","volume":"145","author":"SE Lindsey","year":"2018","journal-title":"Development"},{"issue":"1","key":"pone.0322233.ref016","first-page":"11","article-title":"4-D Computational Modeling of Cardiac Outflow Tract Hemodynamics over Looping Developmental Stages in Chicken Embryos","volume":"6","author":"K Courchaine","year":"2019","journal-title":"J Cardiovasc Dev Dis"},{"issue":"7","key":"pone.0322233.ref017","doi-asserted-by":"crossref","first-page":"1057","DOI":"10.1007\/s10237-012-0373-z","article-title":"Computational hemodynamic optimization predicts dominant aortic arch selection is driven by embryonic outflow tract orientation in the chick embryo","volume":"11","author":"WJ Kowalski","year":"2012","journal-title":"Biomech Model Mechanobiol"},{"issue":"1","key":"pone.0322233.ref018","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1002\/dvdy.22512","article-title":"Hemodynamic patterning of the avian atrioventricular valve","volume":"240","author":"HC Yalcin","year":"2011","journal-title":"Dev Dyn"},{"issue":"3","key":"pone.0322233.ref019","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0060271","article-title":"Critical transitions in early embryonic aortic arch patterning and hemodynamics","volume":"8","author":"WJ Kowalski","year":"2013","journal-title":"PLoS One"},{"issue":"10","key":"pone.0322233.ref020","doi-asserted-by":"crossref","first-page":"2212","DOI":"10.1007\/s10439-012-0574-8","article-title":"Computational fluid dynamics of developing avian outflow tract heart valves","volume":"40","author":"KN Bharadwaj","year":"2012","journal-title":"Ann Biomed Eng"},{"issue":"1","key":"pone.0322233.ref021","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.cjcpc.2023.10.012","article-title":"Advances in Fetal Cardiac Imaging and Intervention","volume":"3","author":"N Barber","year":"2023","journal-title":"CJC Pediatr Congenit Heart Dis"},{"issue":"2","key":"pone.0322233.ref022","first-page":"14","article-title":"Computational Modeling of Blood Flow Hemodynamics for Biomechanical Investigation of Cardiac Development and Disease","volume":"8","author":"HE Salman","year":"2021","journal-title":"J Cardiovasc Dev Dis"},{"key":"pone.0322233.ref023","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-3-319-33038-9_119-1","article-title":"Morphometrics in Evolutionary Developmental Biology","volume-title":"Evolutionary Developmental Biology","author":"P Mitteroecker","year":"2020"},{"key":"pone.0322233.ref024","doi-asserted-by":"crossref","DOI":"10.1002\/9781119072492","volume-title":"Statistical Shape Analysis: With Applications in R","author":"IL Dryden","year":"2016"},{"issue":"3","key":"pone.0322233.ref025","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1111\/jeb.12311","article-title":"Nonlinear effects of temperature on body form and developmental canalization in the threespine stickleback","volume":"27","author":"D Ramler","year":"2014","journal-title":"J Evol Biol"},{"issue":"4","key":"pone.0322233.ref026","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1002\/wdev.98","article-title":"Cardiac outflow tract anomalies","volume":"2","author":"Z Neeb","year":"2013","journal-title":"Wiley Interdiscip Rev Dev Biol"},{"key":"pone.0322233.ref027","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/S0168-3659(97)00103-X","article-title":"Finite element analysis of diffusional drug release from complex matrix systems. I","volume":"49","author":"Y Zhou","year":"1997","journal-title":"Journal of Controlled Release"},{"issue":"4","key":"pone.0322233.ref028","first-page":"32","article-title":"Mechanosensitive Pathways in Heart Development: Findings from Chick Embryo Studies","volume":"8","author":"M Alser","year":"2021","journal-title":"J Cardiovasc Dev Dis"},{"issue":"3","key":"pone.0322233.ref029","doi-asserted-by":"crossref","DOI":"10.1152\/ajpheart.00641.2016","article-title":"Blood flow patterns underlie developmental heart defects","volume":"312","author":"M Midgett","year":"2017","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"pone.0322233.ref030","first-page":"56","article-title":"Increased Hemodynamic Load in Early Embryonic Stages Alters Endocardial to Mesenchymal Transition","volume":"8","author":"M Midgett","year":"2017","journal-title":"Front Physiol"},{"issue":"1","key":"pone.0322233.ref031","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0008-6363(98)00218-1","article-title":"Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal","volume":"41","author":"B Hogers","year":"1999","journal-title":"Cardiovasc Res"},{"key":"pone.0322233.ref032","doi-asserted-by":"crossref","first-page":"318","DOI":"10.3389\/fphys.2014.00318","article-title":"Mechanical regulation of cardiac development","volume":"5","author":"SE Lindsey","year":"2014","journal-title":"Front Physiol"},{"issue":"3","key":"pone.0322233.ref033","doi-asserted-by":"crossref","first-page":"184","DOI":"10.30802\/AALAS-CM-18-000061","article-title":"Embryonic Chicken (Gallus gallus domesticus) as a Model of Cardiac Biology and Development","volume":"69","author":"JG Vilches-Moure","year":"2019","journal-title":"Comp Med"},{"issue":"8","key":"pone.0322233.ref034","first-page":"306","article-title":"Windowing chicken eggs for developmental studies","author":"MJ Korn","year":"2007","journal-title":"J Vis Exp"},{"issue":"4","key":"pone.0322233.ref035","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1007\/s10237-014-0633-1","article-title":"Growth and hemodynamics after early embryonic aortic arch occlusion","volume":"14","author":"SE Lindsey","year":"2015","journal-title":"Biomech Model Mechanobiol"},{"issue":"12","key":"pone.0322233.ref036","doi-asserted-by":"crossref","first-page":"3227","DOI":"10.1007\/s10439-021-02802-2","article-title":"Assessing Early Cardiac Outflow Tract Adaptive Responses Through Combined Experimental-Computational Manipulations","volume":"49","author":"SE Lindsey","year":"2021","journal-title":"Ann Biomed Eng"},{"issue":"6","key":"pone.0322233.ref037","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1007\/s10439-009-9682-5","article-title":"Aortic arch morphogenesis and flow modeling in the chick embryo","volume":"37","author":"Y Wang","year":"2009","journal-title":"Ann Biomed Eng"},{"issue":"1","key":"pone.0322233.ref038","doi-asserted-by":"crossref","first-page":"16948","DOI":"10.1038\/s41598-018-35127-7","article-title":"Asymmetry in Mechanosensitive Gene Expression during Aortic Arch Morphogenesis","volume":"8","author":"C Karakaya","year":"2018","journal-title":"Sci Rep"},{"issue":"4","key":"pone.0322233.ref039","article-title":"Heart disease and stroke statistics--2011 update: a report from the American Heart Association","volume":"123","author":"VL Roger","year":"2011","journal-title":"Circulation"},{"issue":"157","key":"pone.0322233.ref040","doi-asserted-by":"crossref","DOI":"10.3791\/60797","article-title":"Visualization and Analysis of Pharyngeal Arch Arteries using Whole-mount Immunohistochemistry and 3D Reconstruction","author":"A Ramirez","year":"2020","journal-title":"J Vis Exp"},{"key":"pone.0322233.ref041","doi-asserted-by":"crossref","first-page":"408","DOI":"10.3389\/fphys.2014.00408","article-title":"Investigating developmental cardiovascular biomechanics and the origins of congenital heart defects","volume":"5","author":"WJ Kowalski","year":"2014","journal-title":"Front Physiol"},{"issue":"1","key":"pone.0322233.ref042","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1161\/01.CIR.75.1.255","article-title":"Pathogenesis of persistent truncus arteriosus and dextroposed aorta in the chick embryo after neural crest ablation","volume":"75","author":"M Nishibatake","year":"1987","journal-title":"Circulation"},{"issue":"5","key":"pone.0322233.ref043","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1161\/01.RES.59.5.545","article-title":"Hemodynamic changes in chick embryos precede heart defects after cardiac neural crest ablation","volume":"59","author":"DE Stewart","year":"1986","journal-title":"Circ Res"},{"issue":"5","key":"pone.0322233.ref044","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1177\/002215540305100505","article-title":"Selective binding of lectins to embryonic chicken vasculature","volume":"51","author":"SM Jilani","year":"2003","journal-title":"J Histochem Cytochem"},{"issue":"8","key":"pone.0322233.ref045","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.1177\/0003702818778851","article-title":"Recent Progress in Light Sheet Microscopy for Biological Applications","volume":"72","author":"K Chatterjee","year":"2018","journal-title":"Appl Spectrosc"},{"issue":"1","key":"pone.0322233.ref046","article-title":"Light sheet fluorescence microscopy","volume":"1","author":"EHK Stelzer","year":"2021","journal-title":"Nat Rev Methods Primers"},{"issue":"5","key":"pone.0322233.ref047","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1369\/0022155413478613","article-title":"MicroCT versus sTSLIM 3D imaging of the mouse cochlea","volume":"61","author":"JAN Buytaert","year":"2013","journal-title":"J Histochem Cytochem"},{"key":"pone.0322233.ref048","doi-asserted-by":"crossref","first-page":"22489","DOI":"10.1038\/srep22489","article-title":"Cardiac Light-Sheet Fluorescent Microscopy for Multi-Scale and Rapid Imaging of Architecture and Function","volume":"6","author":"P Fei","year":"2016","journal-title":"Sci Rep"},{"issue":"10","key":"pone.0322233.ref049","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1005828","article-title":"A method to quantify mechanobiologic forces during zebrafish cardiac development using 4-D light sheet imaging and computational modeling","volume":"13","author":"V Vedula","year":"2017","journal-title":"PLoS Comput Biol"},{"issue":"4","key":"pone.0322233.ref050","doi-asserted-by":"crossref","first-page":"102387","DOI":"10.1016\/j.isci.2021.102387","article-title":"Tissue clearing and imaging methods for cardiovascular development","volume":"24","author":"H Kolesov\u00e1","year":"2021","journal-title":"iScience"},{"issue":"4","key":"pone.0322233.ref051","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1016\/j.cell.2014.10.010","article-title":"iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging","volume":"159","author":"N Renier","year":"2014","journal-title":"Cell"},{"key":"pone.0322233.ref052"},{"key":"pone.0322233.ref053","first-page":"1","volume-title":"Meshmixer: an interface for rapid mesh composition","author":"R Schmidt","year":"2010"},{"key":"pone.0322233.ref054","author":"Foundation B."},{"key":"pone.0322233.ref055","author":"Quad Remesher - Auto Retopology."},{"key":"pone.0322233.ref056"},{"issue":"2","key":"pone.0322233.ref057","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/s11692-009-9055-x","article-title":"Advances in Geometric Morphometrics","volume":"36","author":"P Mitteroecker","year":"2009","journal-title":"Evol Biol"},{"issue":"4","key":"pone.0322233.ref058","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1007\/s11692-015-9317-8","article-title":"Integration, Disintegration, and Self-Similarity: Characterizing the Scales of Shape Variation in Landmark Data","volume":"42","author":"FL Bookstein","year":"2015","journal-title":"Evol Biol"},{"issue":"9","key":"pone.0322233.ref059","doi-asserted-by":"crossref","first-page":"1323","DOI":"10.1016\/j.mri.2012.05.001","article-title":"3D Slicer as an image computing platform for the Quantitative Imaging Network","volume":"30","author":"A Fedorov","year":"2012","journal-title":"Magn Reson Imaging"},{"key":"pone.0322233.ref060","volume-title":"SlicerMorph: An open and extensible platform to retrieve, visualize and analyze 3D morphology","author":"S Rolfe","year":"2020"},{"issue":"1","key":"pone.0322233.ref061","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1002\/ajpa.24214","article-title":"Comparing semi-landmarking approaches for analyzing three-dimensional cranial morphology","volume":"175","author":"S Rolfe","year":"2021","journal-title":"Am J Phys Anthropol"},{"issue":"11","key":"pone.0322233.ref062","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1111\/2041-210X.13689","article-title":"ALPACA: A fast and accurate computer vision approach for automated landmarking of three-dimensional biological structures","volume":"12","author":"A Porto","year":"2021","journal-title":"Methods Ecol Evol"},{"issue":"8","key":"pone.0322233.ref063","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1109\/TMI.2009.2021652","article-title":"A framework for geometric analysis of vascular structures: application to cerebral aneurysms","volume":"28","author":"M Piccinelli","year":"2009","journal-title":"IEEE Trans Med Imaging"},{"issue":"6","key":"pone.0322233.ref064","doi-asserted-by":"crossref","DOI":"10.1152\/ajpheart.00475.2011","article-title":"Rheology of embryonic avian blood","volume":"301","author":"S Al-Roubaie","year":"2011","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"pone.0322233.ref065","first-page":"279","volume-title":"The libMesh Finite Element Library","author":"BS Kirk"},{"key":"pone.0322233.ref066","author":"S Balay","year":"2022"},{"key":"pone.0322233.ref067","doi-asserted-by":"crossref","DOI":"10.1007\/978-1-4612-3172-1","volume-title":"Mixed and Hybrid Finite Element Methods","author":"F Brezzi","year":"1991"},{"issue":"3","key":"pone.0322233.ref068","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1007\/BF01436561","article-title":"The finite element method with Lagrangian multipliers","volume":"20","author":"I Babu\u0161ka","year":"1973","journal-title":"Numer Math"},{"issue":"8","key":"pone.0322233.ref069","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a037218","article-title":"The Chicken as a Model Organism to Study Heart Development","volume":"12","author":"JG Wittig","year":"2020","journal-title":"Cold Spring Harb Perspect Biol"},{"issue":"4","key":"pone.0322233.ref070","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1002\/(SICI)1097-0185(20000401)258:4<319::AID-AR1>3.0.CO;2-O","article-title":"Developmental patterning of the myocardium","volume":"258","author":"D Sedmera","year":"2000","journal-title":"Anat Rec"},{"issue":"6","key":"pone.0322233.ref071","doi-asserted-by":"crossref","first-page":"1040","DOI":"10.1111\/joa.14017","article-title":"The changing morphology of the ventricular walls of mouse and human with increasing gestation","volume":"244","author":"B Jensen","year":"2024","journal-title":"J Anat"},{"issue":"5","key":"pone.0322233.ref072","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1161\/01.RES.76.5.871","article-title":"Intracardiac blood flow patterns related to the yolk sac circulation of the chick embryo","volume":"76","author":"B Hogers","year":"1995","journal-title":"Circ Res"},{"key":"pone.0322233.ref073","doi-asserted-by":"crossref","first-page":"408","DOI":"10.3389\/fphys.2014.00408","article-title":"Investigating developmental cardiovascular biomechanics and the origins of congenital heart defects","volume":"5","author":"WJ Kowalski","year":"2014","journal-title":"Front Physiol"},{"issue":"3","key":"pone.0322233.ref074","article-title":"Alterations in pulse wave propagation reflect the degree of outflow tract banding in HH18 chicken embryos","volume":"305","author":"L Shi","year":"2013","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"pone.0322233.ref075","first-page":"1","article-title":"Remote large data visualization in the paraview framework","volume":"75","author":"A Cedilnik","year":"2023","journal-title":"Journal Title Abbreviation Needed"},{"issue":"138","key":"pone.0322233.ref076","first-page":"57763","article-title":"Light-sheet Fluorescence Microscopy to Capture 4-Dimensional Images of the Effects of Modulating Shear Stress on the Developing Zebrafish Heart","author":"V Messerschmidt","year":"2018","journal-title":"J Vis Exp"},{"issue":"1","key":"pone.0322233.ref077","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.jmoldx.2011.08.002","article-title":"RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues","volume":"14","author":"F Wang","year":"2012","journal-title":"J Mol Diagn"},{"issue":"6724","key":"pone.0322233.ref078","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1126\/science.adn9947","article-title":"Whole-brain spatial transcriptional analysis at cellular resolution","volume":"386","author":"S Kanatani","year":"2024","journal-title":"Science"},{"issue":"1","key":"pone.0322233.ref079","doi-asserted-by":"crossref","first-page":"18072","DOI":"10.1038\/s41598-019-54061-w","article-title":"Organ Dynamics and Hemodynamic of the Whole HH25 Avian Embryonic Heart, Revealed by Ultrasound Biomicroscopy, Boundary Tracking, and Flow Simulations","volume":"9","author":"S Ho","year":"2019","journal-title":"Sci Rep"},{"issue":"170","key":"pone.0322233.ref080","doi-asserted-by":"crossref","first-page":"20200232","DOI":"10.1098\/rsif.2020.0232","article-title":"Uncertainty quantification reveals the physical constraints on pumping by peristaltic hearts","volume":"17","author":"LD Waldrop","year":"2020","journal-title":"J R Soc Interface"},{"key":"pone.0322233.ref081","doi-asserted-by":"crossref","first-page":"1164345","DOI":"10.3389\/fcvm.2023.1164345","article-title":"Uncertainty quantification of computational fluid dynamics-based predictions for fractional flow reserve and wall shear stress of the idealized stenotic coronary","volume":"10","author":"NN Ho","year":"2023","journal-title":"Front Cardiovasc Med"},{"issue":"12","key":"pone.0322233.ref082","doi-asserted-by":"crossref","first-page":"2540","DOI":"10.1016\/j.jbiomech.2016.01.002","article-title":"Uncertainty quantification in coronary blood flow simulations: Impact of geometry, boundary conditions and blood viscosity","volume":"49","author":"S Sankaran","year":"2016","journal-title":"J Biomech"},{"key":"pone.0322233.ref083","doi-asserted-by":"crossref","first-page":"113030","DOI":"10.1016\/j.cma.2020.113030","article-title":"Multilevel and multifidelity uncertainty quantification for cardiovascular hemodynamics","volume":"365","author":"CM Fleeter","year":"2020","journal-title":"Comput Methods Appl Mech Eng"},{"issue":"1","key":"pone.0322233.ref084","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1002\/jmor.1050880104","article-title":"A series of normal stages in the development of the chick embryo","volume":"88","author":"V Hamburger","year":"1951","journal-title":"Journal of Morphology"},{"issue":"4","key":"pone.0322233.ref085","doi-asserted-by":"crossref","first-page":"1217","DOI":"10.1002\/dvdy.20468","article-title":"Reference guide to the stages of chick heart embryology","volume":"233","author":"BJ Martinsen","year":"2005","journal-title":"Dev Dyn"},{"issue":"5","key":"pone.0322233.ref086","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1007\/BF00304427","article-title":"Formation of the pharyngeal arch arteries in the chick embryo. Observations of corrosion casts by scanning electron microscopy","volume":"191","author":"T Hiruma","year":"1995","journal-title":"Anat Embryol (Berl)"},{"issue":"2","key":"pone.0322233.ref087","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1369\/0022155410394857","article-title":"Light sheet fluorescence microscopy: a review","volume":"59","author":"PA Santi","year":"2011","journal-title":"J Histochem Cytochem"},{"issue":"7","key":"pone.0322233.ref088","doi-asserted-by":"crossref","DOI":"10.1002\/cpz1.448","article-title":"Lightsheet Microscopy","volume":"2","author":"L Dyer","year":"2022","journal-title":"Curr Protoc"},{"key":"pone.0322233.ref089"},{"issue":"11","key":"pone.0322233.ref090","doi-asserted-by":"crossref","first-page":"1097","DOI":"10.1007\/s11517-008-0420-1","article-title":"An image-based modeling framework for patient-specific computational hemodynamics","volume":"46","author":"L Antiga","year":"2008","journal-title":"Med Biol Eng Comput"},{"key":"pone.0322233.ref091","volume-title":"Integration of The Vascular Modeling Toolkit in 3D Slicer","author":"D H\u00e4hn","year":"2009"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0322233","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,5,19]],"date-time":"2025-05-19T17:51:13Z","timestamp":1747677073000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0322233"}},"subtitle":[],"editor":[{"given":"Ad\u00e9lia","family":"Sequeira","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,5,19]]},"references-count":91,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,5,19]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0322233","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,19]]}}}