{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T19:14:58Z","timestamp":1792782898765,"version":"4.5.0"},"reference-count":62,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2021,1,22]],"date-time":"2021-01-22T00:00:00Z","timestamp":1611273600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,1,22]],"date-time":"2021-01-22T00:00:00Z","timestamp":1611273600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100008982","name":"Qatar National Research Fund","doi-asserted-by":"publisher","award":["NPRP 10-0123-170222"],"award-info":[{"award-number":["NPRP 10-0123-170222"]}],"id":[{"id":"10.13039\/100008982","id-type":"DOI","asserted-by":"publisher"}]},{"name":"National Science Foundation","award":["NSF CMMI 1635712"],"award-info":[{"award-number":["NSF CMMI 1635712"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Biomech Model Mechanobiol"],"published-print":{"date-parts":[[2021,4]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Congenital heart defects (CHDs) are abnormalities in the heart structure present at birth. One important condition is hypoplastic left heart syndrome (HLHS) where severely underdeveloped left ventricle (LV) cannot support systemic circulation. HLHS usually initiates as localized tissue malformations with no underlying genetic cause, suggesting that disturbed hemodynamics contribute to the embryonic development of these defects. Left atrial ligation (LAL) is a surgical procedure on embryonic chick resulting in a phenotype resembling clinical HLHS. In this study, we investigated disturbed hemodynamics and deteriorated cardiac growth following LAL to investigate possible mechanobiological mechanisms for the embryonic development of HLHS. We integrated techniques such as echocardiography, micro-CT and computational fluid dynamics (CFD) for these analyses. Specifically, LAL procedure causes an immediate flow disturbance over atrioventricular (AV) cushions. At later stages after the heart septation, it causes hemodynamic disturbances in LV. As a consequence of the LAL procedure, the left-AV canal and LV volume decrease in size, and in the opposite way, the right-AV canal and right ventricle volume increase. According to our CFD analysis, LAL results in an immediate decrease in the left AV canal WSS levels for 3.5-day (HH21) pre-septated hearts. For 7-day post-septated hearts (HH30), LAL leads to further reduction in WSS levels in the left AV canal, and relatively increased WSS levels in the right AV canal. This study demonstrates the critical importance of the disturbed hemodynamics during the heart valve and ventricle development.<\/jats:p>","DOI":"10.1007\/s10237-020-01413-5","type":"journal-article","created":{"date-parts":[[2021,1,22]],"date-time":"2021-01-22T06:09:26Z","timestamp":1611295766000},"page":"733-750","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":36,"title":["Effect of left atrial ligation-driven altered inflow hemodynamics on embryonic heart development: clues for prenatal progression of hypoplastic left heart syndrome"],"prefix":"10.1007","volume":"20","author":[{"given":"Huseyin Enes","family":"Salman","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maha","family":"Alser","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Akshay","family":"Shekhar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Russell A.","family":"Gould","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fatiha M.","family":"Benslimane","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan T.","family":"Butcher","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huseyin C.","family":"Yalcin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,1,22]]},"reference":[{"key":"1413_CR1","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1002\/dvdy.20367","volume":"233","author":"T Bartman","year":"2005","unstructured":"Bartman T, Hove J (2005) Mechanics and function in heart morphogenesis. Dev Dyn 233:373\u2013381. https:\/\/doi.org\/10.1002\/dvdy.20367","journal-title":"Dev Dyn"},{"key":"1413_CR2","doi-asserted-by":"publisher","first-page":"96","DOI":"10.3389\/fbioe.2019.00096","volume":"7","author":"FM Benslimane","year":"2019","unstructured":"Benslimane FM, Alser M, Zakaria ZZ, Sharma A, Abdelrahman HA, Yalcin HC (2019) Adaptation of a mice doppler echocardiography platform to measure cardiac flow velocities for embryonic chicken and adult zebrafish. Front Bioeng Biotechnol 7:96. https:\/\/doi.org\/10.3389\/fbioe.2019.00096","journal-title":"Front Bioeng Biotechnol"},{"key":"1413_CR3","doi-asserted-by":"publisher","first-page":"102876","DOI":"10.1016\/j.micron.2020.102876","volume":"136","author":"FM Benslimane","year":"2020","unstructured":"Benslimane FM, Zakaria ZZ, Shurbaji S, Abdelrasool MKA, Al-Badr MAHI, Al Absi ESK, Yalcin HC (2020) Cardiac function and blood flow hemodynamics assessment of zebrafish (Danio rerio) using high-speed video microscopy. Micron 136:102876. https:\/\/doi.org\/10.1016\/j.micron.2020.102876","journal-title":"Micron"},{"key":"1413_CR4","doi-asserted-by":"publisher","first-page":"2212","DOI":"10.1007\/s10439-012-0574-8","volume":"40","author":"KN Bharadwaj","year":"2012","unstructured":"Bharadwaj KN, Spitz C, Shekhar A, Yalcin HC, Butcher JT (2012) Computational fluid dynamics of developing avian outflow tract heart valves. Ann Biomed Eng 40:2212\u20132227. https:\/\/doi.org\/10.1007\/s10439-012-0574-8","journal-title":"Ann Biomed Eng"},{"key":"1413_CR5","first-page":"335","volume":"95","author":"SM Bradley","year":"1999","unstructured":"Bradley SM (1999) Neonatal repair and dealing with a single ventricle. J S C Med Assoc 95:335\u2013338","journal-title":"J S C Med Assoc"},{"key":"1413_CR6","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1086\/422230","volume":"77","author":"WW Burggren","year":"2004","unstructured":"Burggren WW (2004) What is the purpose of the embryonic heart beat? or how facts can ultimately prevail over physiological dogma. Physiol Biochem Zool 77:333\u2013345. https:\/\/doi.org\/10.1086\/422230","journal-title":"Physiol Biochem Zool"},{"key":"1413_CR7","doi-asserted-by":"publisher","first-page":"1503","DOI":"10.1161\/CIRCRESAHA.107.148684","volume":"100","author":"JT Butcher","year":"2007","unstructured":"Butcher JT, McQuinn Tim C, Sedmera D, Turner D, Markwald Roger R (2007) Transitions in early embryonic atrioventricular valvular function correspond with changes in cushion biomechanics that are predictable by tissue composition. Circ Res 100:1503\u20131511. https:\/\/doi.org\/10.1161\/CIRCRESAHA.107.148684","journal-title":"Circ Res"},{"key":"1413_CR8","doi-asserted-by":"publisher","first-page":"H55","DOI":"10.1152\/ajpheart.1989.257.1.h55","volume":"257","author":"EB Clark","year":"1989","unstructured":"Clark EB, Hu N, Frommelt P, Vandekieft GK, Dummett JL, Tomanek RJ (1989) Effect of increased pressure on ventricular growth in stage 21 chick embryos. Am J Physiol Heart Circ Physiol 257:H55\u2013H61. https:\/\/doi.org\/10.1152\/ajpheart.1989.257.1.h55","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"1413_CR9","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1111\/j.1549-8719.2010.00025.x","volume":"17","author":"JC Culver","year":"2010","unstructured":"Culver JC, Dickinson ME (2010) The effects of hemodynamic force on embryonic development. Microcirculation 17:164\u2013178. https:\/\/doi.org\/10.1111\/j.1549-8719.2010.00025.x","journal-title":"Microcirculation"},{"key":"1413_CR10","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1002\/ar.20808","volume":"292","author":"A Davis","year":"2009","unstructured":"Davis A, Izatt J, Rothenberg F (2009) Quantitative measurement of blood flow dynamics in embryonic vasculature using spectral doppler velocimetry. Anat Rec 292:311\u2013319. https:\/\/doi.org\/10.1002\/ar.20808","journal-title":"Anat Rec"},{"key":"1413_CR11","doi-asserted-by":"publisher","first-page":"1363","DOI":"10.1161\/01.RES.0000266606.88463.cb","volume":"100","author":"A deAlmeida","year":"2007","unstructured":"deAlmeida A, McQuinn T, Sedmera D (2007) Increased ventricular preload is compensated by myocyte proliferation in normal and hypoplastic fetal chick left ventricle. Circ Res 100:1363\u20131370. https:\/\/doi.org\/10.1161\/01.RES.0000266606.88463.cb","journal-title":"Circ Res"},{"key":"1413_CR12","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1007\/s00246-001-0196-7","volume":"23","author":"CG DeGroff","year":"2002","unstructured":"DeGroff CG (2002) Doppler echocardiography Pediatr Cardiol 23:307\u2013333. https:\/\/doi.org\/10.1007\/s00246-001-0196-7","journal-title":"Doppler echocardiography Pediatr Cardiol"},{"key":"1413_CR13","doi-asserted-by":"publisher","first-page":"2806","DOI":"10.1161\/ATVBAHA.118.311231","volume":"38","author":"S Eisa-Beygi","year":"2018","unstructured":"Eisa-Beygi S et al (2018) Characterization of endothelial cilia distribution during cerebral-vascular development in zebrafish (Danio rerio). Arterioscler Thromb Vasc Biol 38:2806\u20132818. https:\/\/doi.org\/10.1161\/ATVBAHA.118.311231","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"1413_CR14","doi-asserted-by":"publisher","first-page":"914","DOI":"10.1002\/dvdy.24635","volume":"247","author":"MG Espinosa","year":"2018","unstructured":"Espinosa MG, Taber LA, Wagenseil JE (2018) Reduced embryonic blood flow impacts extracellular matrix deposition in the maturing aorta. Dev Dyn Off Publ Am Assoc Anat 247:914\u2013923. https:\/\/doi.org\/10.1002\/dvdy.24635","journal-title":"Dev Dyn Off Publ Am Assoc Anat"},{"key":"1413_CR15","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1126\/science.1123775","volume":"312","author":"AS Forouhar","year":"2006","unstructured":"Forouhar AS et al (2006) The embryonic vertebrate heart tube is a dynamic suction pump. Science 312:751. https:\/\/doi.org\/10.1126\/science.1123775","journal-title":"Science"},{"key":"1413_CR16","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1161\/circulationaha.114.009032","volume":"130","author":"LR Freud","year":"2014","unstructured":"Freud LR et al (2014) Fetal aortic valvuloplasty for evolving hypoplastic left heart syndrome: postnatal outcomes of the first 100 patients. Circulation 130:638\u2013645. https:\/\/doi.org\/10.1161\/circulationaha.114.009032","journal-title":"Circulation"},{"key":"1413_CR17","doi-asserted-by":"publisher","first-page":"1291","DOI":"10.1161\/01.RES.0000171901.40952.0d","volume":"96","author":"BCW Groenendijk","year":"2005","unstructured":"Groenendijk BCW, Hierck BP, Vrolijk J, Baiker M, Pourquie MJ, Gittenberger-de Groot AC, Poelmann RE (2005) Changes in shear stress\u2013related gene expression after experimentally altered venous return in the chicken embryo. Circ Res 96:1291\u20131298. https:\/\/doi.org\/10.1161\/01.RES.0000171901.40952.0d","journal-title":"Circ Res"},{"key":"1413_CR18","doi-asserted-by":"publisher","first-page":"1949","DOI":"10.1002\/dvdy.22694","volume":"240","author":"AL Henning","year":"2011","unstructured":"Henning AL, Jiang MX, Yalcin HC, Butcher JT (2011) Quantitative three-dimensional imaging of live avian embryonic morphogenesis via micro-computed tomography. Dev Dyn 240:1949\u20131957. https:\/\/doi.org\/10.1002\/dvdy.22694","journal-title":"Dev Dyn"},{"key":"1413_CR19","doi-asserted-by":"publisher","first-page":"141","DOI":"10.5830\/CVJA-2013-028","volume":"24","author":"JI Hoffman","year":"2013","unstructured":"Hoffman JI (2013) The global burden of congenital heart disease. Cardiovasc J Afr 24:141\u2013145. https:\/\/doi.org\/10.5830\/CVJA-2013-028","journal-title":"Cardiovasc J Afr"},{"key":"1413_CR20","doi-asserted-by":"publisher","first-page":"1890","DOI":"10.1016\/S0735-1097(02)01886-7","volume":"39","author":"JIE Hoffman","year":"2002","unstructured":"Hoffman JIE, Kaplan S (2002) The incidence of congenital heart disease. J Am College Cardiol 39:1890. https:\/\/doi.org\/10.1016\/S0735-1097(02)01886-7","journal-title":"J Am College Cardiol"},{"key":"1413_CR21","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1161\/01.res.80.4.473","volume":"80","author":"B Hogers","year":"1997","unstructured":"Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE (1997) Unilateral vitelline vein ligation alters intracardiac blood flow patterns and morphogenesis in the chick embryo. Circ Res 80:473\u2013481. https:\/\/doi.org\/10.1161\/01.res.80.4.473","journal-title":"Circ Res"},{"key":"1413_CR22","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/S0008-6363(98)00218-1","volume":"41","author":"B Hogers","year":"1999","unstructured":"Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE (1999) Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal. Cardiovasc Res 41:87\u201399. https:\/\/doi.org\/10.1016\/S0008-6363(98)00218-1","journal-title":"Cardiovasc Res"},{"key":"1413_CR23","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1038\/nature01282","volume":"421","author":"JR Hove","year":"2003","unstructured":"Hove JR, K\u00f6ster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M (2003) Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421:172\u2013177. https:\/\/doi.org\/10.1038\/nature01282","journal-title":"Nature"},{"key":"1413_CR24","unstructured":"https:\/\/www.nature.com\/articles\/nature12141#supplementary-information"},{"key":"1413_CR25","doi-asserted-by":"publisher","first-page":"1665","DOI":"10.1161\/01.res.65.6.1665","volume":"65","author":"N Hu","year":"1989","unstructured":"Hu N, Clark EB (1989) Hemodynamics of the stage 12 to stage 29 chick embryo. Circ Res 65:1665\u20131670. https:\/\/doi.org\/10.1161\/01.res.65.6.1665","journal-title":"Circ Res"},{"key":"1413_CR26","doi-asserted-by":"publisher","first-page":"652","DOI":"10.1002\/ar.20885","volume":"292","author":"N Hu","year":"2009","unstructured":"Hu N, Christensen DA, Agrawal AK, Beaumont C, Clark EB, Hawkins JA (2009) Dependence of aortic arch morphogenesis on intracardiac blood flow in the left atrial ligated chick embryo. Anat Rec 292:652\u2013660. https:\/\/doi.org\/10.1002\/ar.20885","journal-title":"Anat Rec"},{"key":"1413_CR27","doi-asserted-by":"publisher","first-page":"652","DOI":"10.1002\/dvdy.24107","volume":"243","author":"WJ Kowalski","year":"2014","unstructured":"Kowalski WJ, Teslovich NC, Menon PG, Tinney JP, Keller BB, Pekkan K (2014) Left atrial ligation alters intracardiac flow patterns and the biomechanical landscape in the chick embryo. Dev Dyn 243:652\u2013662. https:\/\/doi.org\/10.1002\/dvdy.24107","journal-title":"Dev Dyn"},{"key":"1413_CR28","doi-asserted-by":"publisher","first-page":"96006","DOI":"10.1117\/1.JBO.17.9.096006","volume":"17","author":"P Li","year":"2012","unstructured":"Li P, Yin X, Shi L, Rugonyi S, Wang RK (2012) vivo functional imaging of blood flow and wall strain rate in outflow tract of embryonic chick heart using ultrafast spectral domain optical coherence tomography. J Biomed Opt 17:96006. https:\/\/doi.org\/10.1117\/1.JBO.17.9.096006","journal-title":"J Biomed Opt"},{"key":"1413_CR29","doi-asserted-by":"publisher","first-page":"520","DOI":"10.1038\/nature14269","volume":"521","author":"Y Li","year":"2015","unstructured":"Li Y et al (2015) Global genetic analysis in mice unveils central role for cilia in congenital heart disease. Nature 521:520\u2013524. https:\/\/doi.org\/10.1038\/nature14269","journal-title":"Nature"},{"key":"1413_CR30","doi-asserted-by":"publisher","first-page":"318","DOI":"10.3389\/fphys.2014.00318","volume":"5","author":"SE Lindsey","year":"2014","unstructured":"Lindsey SE, Butcher JT, Yalcin HC (2014) Mechanical regulation of cardiac development. Front Physiol 5:318","journal-title":"Front Physiol"},{"key":"1413_CR31","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1007\/s10237-014-0633-1","volume":"14","author":"SE Lindsey","year":"2015","unstructured":"Lindsey SE et al (2015) Growth and hemodynamics after early embryonic aortic arch occlusion. Biomech Model Mechanobiol 14:735\u2013751. https:\/\/doi.org\/10.1007\/s10237-014-0633-1","journal-title":"Biomech Model Mechanobiol"},{"key":"1413_CR32","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1016\/j.compstruc.2007.01.014","volume":"85","author":"A Liu","year":"2007","unstructured":"Liu A, Rugonyi S, Pentecost JO, Thornburg KL (2007) Finite element modeling of blood flow-induced mechanical forces in the outflow tract of chick embryonic hearts. Comput Struct 85:727\u2013738. https:\/\/doi.org\/10.1016\/j.compstruc.2007.01.014","journal-title":"Comput Struct"},{"key":"1413_CR33","doi-asserted-by":"publisher","first-page":"3503","DOI":"10.1002\/dvdy.21357","volume":"236","author":"TC McQuinn","year":"2007","unstructured":"McQuinn TC, Bratoeva M, DeAlmeida A, Remond M, Thompson RP, Sedmera D (2007) High-frequency ultrasonographic imaging of avian cardiovascular development. Dev Dyn 236:3503\u20133513. https:\/\/doi.org\/10.1002\/dvdy.21357","journal-title":"Dev Dyn"},{"key":"1413_CR34","doi-asserted-by":"publisher","first-page":"108","DOI":"10.3390\/jcdd2020108","volume":"2","author":"V Menon","year":"2015","unstructured":"Menon V, Eberth J, Goodwin R, Potts J (2015) Altered hemodynamics in the embryonic heart affects outflow valve development. J Cardiovasc Dev Dis 2:108","journal-title":"J Cardiovasc Dev Dis"},{"key":"1413_CR35","doi-asserted-by":"publisher","first-page":"287","DOI":"10.3389\/fphys.2014.00287","volume":"5","author":"M Midgett","year":"2014","unstructured":"Midgett M, Rugonyi S (2014) Congenital heart malformations induced by hemodynamic altering surgical interventions. Front Physiol 5:287","journal-title":"Front Physiol"},{"key":"1413_CR36","doi-asserted-by":"publisher","first-page":"H1849","DOI":"10.1152\/ajpheart.00384.2002","volume":"285","author":"CE Miller","year":"2003","unstructured":"Miller CE, Wong CL, Sedmera D (2003) Pressure overload alters stress-strain properties of the developing chick heart. Am J Physiol Heart Circ Physiol 285:H1849\u2013H1856. https:\/\/doi.org\/10.1152\/ajpheart.00384.2002","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"1413_CR37","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1056\/NEJM198301063080106","volume":"308","author":"WI Norwood","year":"1983","unstructured":"Norwood WI, Lang P, Hansen DD (1983) Physiologic repair of aortic atresia-hypoplastic left heart syndrome. N Engl J Med 308:23\u201326. https:\/\/doi.org\/10.1056\/NEJM198301063080106","journal-title":"N Engl J Med"},{"key":"1413_CR38","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1002\/uog.6362","volume":"33","author":"AM Oosterbaan","year":"2009","unstructured":"Oosterbaan AM, Ursem NTC, Struijk PC, Bosch JG, van der Steen AFW, Steegers EAP (2009) Doppler flow velocity waveforms in the embryonic chicken heart at developmental stages corresponding to 5\u20138\u00a0weeks of human gestation. Ultrasound Obstet Gynecol 33:638\u2013644. https:\/\/doi.org\/10.1002\/uog.6362","journal-title":"Ultrasound Obstet Gynecol"},{"key":"1413_CR39","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1161\/circulationaha.109.857987","volume":"120","author":"N \u00d8yen","year":"2009","unstructured":"\u00d8yen N, Poulsen G, Boyd HA, Wohlfahrt J, Jensen PKA, Melbye M (2009) Recurrence of congenital heart defects in families. Circulation 120:295\u2013301. https:\/\/doi.org\/10.1161\/circulationaha.109.857987","journal-title":"Circulation"},{"key":"1413_CR40","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1161\/01.RES.0000079488.91342.B7","volume":"93","author":"M Reckova","year":"2003","unstructured":"Reckova M et al (2003) Hemodynamics is a key epigenetic factor in development of the cardiac conduction system. Circ Res 93:77\u201385. https:\/\/doi.org\/10.1161\/01.RES.0000079488.91342.B7","journal-title":"Circ Res"},{"key":"1413_CR41","doi-asserted-by":"publisher","first-page":"e18","DOI":"10.1161\/cir.0b013e3182009701","volume":"123","author":"VL Roger","year":"2011","unstructured":"Roger VL et al (2011) Heart disease and stroke statistics\u20142011 update. Circulation 123:e18\u2013e209. https:\/\/doi.org\/10.1161\/cir.0b013e3182009701","journal-title":"Circulation"},{"key":"1413_CR42","doi-asserted-by":"publisher","first-page":"5077","DOI":"10.1088\/0031-9155\/53\/18\/015","volume":"53","author":"S Rugonyi","year":"2008","unstructured":"Rugonyi S, Shaut C, Liu A, Thornburg K, Wang RK (2008) Changes in wall motion and blood flow in the outflow tract of chick embryonic hearts observed with optical coherence tomography after outflow tract banding and vitelline-vein ligation. Phys Med Biol 53:5077\u20135091. https:\/\/doi.org\/10.1088\/0031-9155\/53\/18\/015","journal-title":"Phys Med Biol"},{"key":"1413_CR43","doi-asserted-by":"publisher","first-page":"412","DOI":"10.1016\/S0039-6060(97)90034-9","volume":"122","author":"Y Saiki","year":"1997","unstructured":"Saiki Y, Konig A, Waddell J, Rebeyka IM (1997) Hemodynamic alteration by fetal surgery accelerates myocyte proliferation in fetal guinea pig hearts. Surgery 122:412\u2013419. https:\/\/doi.org\/10.1016\/S0039-6060(97)90034-9","journal-title":"Surgery"},{"key":"1413_CR44","doi-asserted-by":"publisher","first-page":"102801","DOI":"10.1016\/j.micron.2019.102801","volume":"130","author":"HE Salman","year":"2020","unstructured":"Salman HE, Yalcin HC (2020) Advanced blood flow assessment in Zebrafish via experimental digital particle image velocimetry and computational fluid dynamics modeling. Micron 130:102801. https:\/\/doi.org\/10.1016\/j.micron.2019.102801","journal-title":"Micron"},{"key":"1413_CR45","doi-asserted-by":"publisher","first-page":"111","DOI":"10.3389\/fbioe.2019.00111","volume":"7","author":"HE Salman","year":"2019","unstructured":"Salman HE, Ramazanli B, Yavuz MM, Yalcin HC (2019) biomechanical investigation of disturbed hemodynamics-induced tissue degeneration in abdominal aortic aneurysms using computational and experimental techniques. Front Bioeng Biotechnol 7:111. https:\/\/doi.org\/10.3389\/fbioe.2019.00111","journal-title":"Front Bioeng Biotechnol"},{"key":"1413_CR46","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/j.yjmcc.2019.08.005","volume":"135","author":"A Saraf","year":"2019","unstructured":"Saraf A, Book WM, Nelson TJ, Xu C (2019) Hypoplastic left heart syndrome: from bedside to bench and back. J Mol Cell Cardiol 135:109\u2013118. https:\/\/doi.org\/10.1016\/j.yjmcc.2019.08.005","journal-title":"J Mol Cell Cardiol"},{"key":"1413_CR47","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1002\/(SICI)1097-0185(19990201)254:2<238::AID-AR10>3.0.CO;2-V","volume":"254","author":"D Sedmera","year":"1999","unstructured":"Sedmera D, Pexieder T, Rychterova V, Hu N, Clark EB (1999) Remodeling of chick embryonic ventricular myoarchitecture under experimentally changed loading conditions. Anat Rec 254:238\u2013252. https:\/\/doi.org\/10.1002\/(SICI)1097-0185(19990201)254:2%3c238:AID-AR10%3e3.0.CO;2-V","journal-title":"Anat Rec"},{"key":"1413_CR48","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1002\/ar.10098","volume":"267","author":"D Sedmera","year":"2002","unstructured":"Sedmera D, Hu N, Weiss KM, Keller BB, Denslow S, Thompson RP (2002) Cellular changes in experimental left heart hypoplasia. Anat Rec 267:137\u2013145. https:\/\/doi.org\/10.1002\/ar.10098","journal-title":"Anat Rec"},{"key":"1413_CR49","doi-asserted-by":"publisher","first-page":"H386","DOI":"10.1152\/ajpheart.00100.2013","volume":"305","author":"L Shi","year":"2013","unstructured":"Shi L, Goenezen S, Haller S, Hinds MT, Thornburg KL, Rugonyi S (2013) Alterations in pulse wave propagation reflect the degree of outflow tract banding in HH18 chicken embryos. Am J Physiol Heart Circ Physiol 305:H386\u2013H396. https:\/\/doi.org\/10.1152\/ajpheart.00100.2013","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"1413_CR50","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1038\/35025190","volume":"407","author":"D Srivastava","year":"2000","unstructured":"Srivastava D, Olson EN (2000) A genetic blueprint for cardiac development. Nature 407:221\u2013226. https:\/\/doi.org\/10.1038\/35025190","journal-title":"Nature"},{"key":"1413_CR51","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1016\/S0003-4975(99)01283-7","volume":"69","author":"CI Tchervenkov","year":"2000","unstructured":"Tchervenkov CI, Jacobs ML, Tahta SA (2000) Congenital heart surgery nomenclature and database project: hypoplastic left heart syndrome. Ann Thorac Surg 69:170\u2013179. https:\/\/doi.org\/10.1016\/S0003-4975(99)01283-7","journal-title":"Ann Thorac Surg"},{"key":"1413_CR52","doi-asserted-by":"publisher","first-page":"H959","DOI":"10.1152\/ajpheart.2000.279.3.H959","volume":"279","author":"K Tobita","year":"2000","unstructured":"Tobita K, Keller BB (2000) Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos. Am J Physiol Heart Circ Physiol 279:H959\u2013H969. https:\/\/doi.org\/10.1152\/ajpheart.2000.279.3.H959","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"1413_CR53","doi-asserted-by":"publisher","first-page":"H2386","DOI":"10.1152\/ajpheart.00879.2001","volume":"282","author":"K Tobita","year":"2002","unstructured":"Tobita K, Schroder EA, Tinney JP, Garrison JB, Keller BB (2002) Regional passive ventricular stress-strain relations during development of altered loads in chick embryo. Am J Physiol Heart Circ Physiol 282:H2386\u2013H2396. https:\/\/doi.org\/10.1152\/ajpheart.00879.2001","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"1413_CR54","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1002\/ar.a.20133","volume":"283A","author":"K Tobita","year":"2005","unstructured":"Tobita K, Garrison JB, Liu LJ, Tinney JP, Keller BB (2005) Three-dimensional myofiber architecture of the embryonic left ventricle during normal development and altered mechanical loads. Anat Rec Part A Discov Mol Cell Evol Biol 283A:193\u2013201. https:\/\/doi.org\/10.1002\/ar.a.20133","journal-title":"Anat Rec Part A Discov Mol Cell Evol Biol"},{"key":"1413_CR55","doi-asserted-by":"publisher","first-page":"2125","DOI":"10.1161\/01.CIR.0000144357.29279.54","volume":"110","author":"W Tworetzky","year":"2004","unstructured":"Tworetzky W et al (2004) Balloon dilation of severe aortic stenosis in the fetus. Circulation 110:2125\u20132131. https:\/\/doi.org\/10.1161\/01.CIR.0000144357.29279.54","journal-title":"Circulation"},{"key":"1413_CR56","doi-asserted-by":"publisher","first-page":"1644","DOI":"10.1177\/1535370214546272","volume":"239","author":"HC Yalcin","year":"2014","unstructured":"Yalcin HC (2014) Femtosecond laser photodisruption of vitelline vessels of avian embryos as a technique to study embryonic vascular remodeling. Exp Biol Med 239:1644\u20131652. https:\/\/doi.org\/10.1177\/1535370214546272","journal-title":"Exp Biol Med"},{"key":"1413_CR57","doi-asserted-by":"publisher","first-page":"H1728","DOI":"10.1152\/ajpheart.00495.2010","volume":"299","author":"HC Yalcin","year":"2010","unstructured":"Yalcin HC, Shekhar A, Nishimura N, Rane AA, Schaffer CB, Butcher JT (2010a) Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects. Am J Physiol Heart Circ Physiol 299:H1728\u2013H1735. https:\/\/doi.org\/10.1152\/ajpheart.00495.2010","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"1413_CR58","doi-asserted-by":"publisher","DOI":"10.3791\/2154","author":"HC Yalcin","year":"2010","unstructured":"Yalcin HC, Shekhar A, Rane AA, Butcher JT (2010b) An ex-ovo chicken embryo culture system suitable for imaging and microsurgery applications. JoVE. https:\/\/doi.org\/10.3791\/2154","journal-title":"JoVE"},{"key":"1413_CR59","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1002\/dvdy.22512","volume":"240","author":"HC Yalcin","year":"2011","unstructured":"Yalcin HC, Shekhar A, McQuinn TC, Butcher JT (2011) Hemodynamic patterning of the avian atrioventricular valve. Dev Dyn 240:23\u201335. https:\/\/doi.org\/10.1002\/dvdy.22512","journal-title":"Dev Dyn"},{"key":"1413_CR60","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1002\/dvdy.24497","volume":"246","author":"HC Yalcin","year":"2017","unstructured":"Yalcin HC, Amindari A, Butcher JT, Althani A, Yacoub M (2017) Heart function and hemodynamic analysis for zebrafish embryos. Dev Dyn 246:868\u2013880. https:\/\/doi.org\/10.1002\/dvdy.24497","journal-title":"Dev Dyn"},{"key":"1413_CR61","doi-asserted-by":"publisher","first-page":"220","DOI":"10.1038\/nature12141","volume":"498","author":"S Zaidi","year":"2013","unstructured":"Zaidi S et al (2013) De novo mutations in histone-modifying genes in congenital heart disease. Nature 498:220. https:\/\/doi.org\/10.1038\/nature12141","journal-title":"Nature"},{"key":"1413_CR62","doi-asserted-by":"publisher","first-page":"1642684","DOI":"10.1155\/2018\/1642684","volume":"2018","author":"ZZ Zakaria","year":"2018","unstructured":"Zakaria ZZ et al (2018) Using zebrafish for investigating the molecular mechanisms of drug-induced cardiotoxicity. Biomed Res Int 2018:1642684. https:\/\/doi.org\/10.1155\/2018\/1642684","journal-title":"Biomed Res Int"}],"container-title":["Biomechanics and Modeling in Mechanobiology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s10237-020-01413-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s10237-020-01413-5\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s10237-020-01413-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,3,19]],"date-time":"2021-03-19T10:26:56Z","timestamp":1616149616000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s10237-020-01413-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,22]]},"references-count":62,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2021,4]]}},"alternative-id":["1413"],"URL":"https:\/\/doi.org\/10.1007\/s10237-020-01413-5","relation":{},"ISSN":["1617-7959","1617-7940"],"issn-type":[{"value":"1617-7959","type":"print"},{"value":"1617-7940","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,22]]},"assertion":[{"value":"2 June 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 December 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 January 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"Embryonic chick experiments were performed under QU-IACUC 1-12\/2017 approval from Qatar University.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"The authors declare that they have no conflict of interest.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflicts of interest"}}]}}