Biomechanics of early cardiac development

Biomechanics and Modeling in Mechanobiology

Volumn 11, Issue 8, 2012, Pages 1187-1204

  Goenezen, Sevan ^a   Rennie, Monique Y ^b   Rugonyi, Sandra ^a  

^a Oregon Health and Science University Department of Biomedical Engineering   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Blood flow modeling; Cardiogenesis; Computational biomechanics; Computational modeling; Early cardiac development; Valveless pumping

Indexed keywords

BEHAVIORAL RESEARCH; BIOMECHANICS; BIOPHYSICS; COMPUTATION THEORY; HEART;

BLOOD FLOW MODELING; CARDIOGENESIS; COMPUTATIONAL BIOMECHANICS; COMPUTATIONAL MODELLING; CONGENITAL HEART DEFECTS; EARLY CARDIAC DEVELOPMENT; HAEMODYNAMICS; HEMODYNAMIC FORCES; VALVELESS PUMPING; WEALTH OF INFORMATION;

HEMODYNAMICS;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; EMBRYO DEVELOPMENT; EXTRACELLULAR MATRIX; GROWTH, DEVELOPMENT AND AGING; HEART; HUMAN; MECHANICAL STRESS; MECHANOTRANSDUCTION; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; COMPUTER SIMULATION; EMBRYONIC DEVELOPMENT; EXTRACELLULAR MATRIX; HEART; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; STRESS, MECHANICAL;

EID: 84870833342     PISSN: 16177959     EISSN: 16177940     Source Type: Journal    
DOI: 10.1007/s10237-012-0414-7     Document Type: Article

References (167)

1. Abu-Daya A, Sater AK, Wells DE, Mohun TJ, Zimmerman LB (2009) Absence of heartbeat in the Xenopus tropicalis mutation muzak is caused by a nonsense mutation in cardiac myosin myh6. Dev Biol 336(1):20-29
2. Avrahami I, Gharib M (2008) Computational studies of resonancewave pumping in compliant tubes. J Fluid Mech 608:139-160 (Pubitemid 352044200)
3. Baker K, Holtzman NG, Burdine RD (2008) Direct and indirect roles for nodal signaling in two axis conversions during asymmetric morphogenesis of the zebrafish heart. Proc Natl Acad Sci USA 105(37):13924-13929
4. Bakkers J (2011) Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res 91(2):279-288
5. Barry A (1942) The intrinsic pulsation rates of fragments of the embryonic chick heart. J Exp Zool 91(2):119-130
6. Barry A (1948) The functional significance of the cardiac jelly in the tubular heart of the chick embryo. Anat Rec 102(3):289-298
7. Bartman T, Hove J (2005) Mechanics and function in heart morphogenesis. Dev Dyn 233(2):373-381 (Pubitemid 40734039)
8. Benson JDW, Hughes SF, Hu N, Clark EB (1989) Effect of heart rate increase on dorsal aortic flow before and after volume loading in the stage 24 chick embryo. Pediatr Res 26(5):438-441 (Pubitemid 19267293)
9. Biechler SV, Potts JD, Yost MJ, Junor L, Goodwin RL, Weidner JW (2010) Mathematical modeling of flow-generated forces in an in vitro system of cardiac valve development. Ann Biomed Eng 38(1):109-117
10. Bogue JY (1932) The heart rate of the developing chick. J Exp Biol 9:351-358
11. Bouman H, Broekhuizen M, Baasten A, Gittenberger-DeGroot A, Wenink A (1995) Spectrum of looping disturbances in stage 34 chicken hearts after retinoic acid treatment. Anat Rec 243(1):101-108
12. Bremer JL (1932) The presence and influence of two spiral streams in the heart of the chick embryo. Am J Anat 49(3):409-440
13. Broekhuizen ML, Hogers B, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC, Wladimiroff JW (1999) Altered hemodynamics in chick embryos after extraembryonic venous obstruction. Ultrasound Obstet Gynecol 13(6):437-445 (Pubitemid 29363899)
14. Bruneau BG (2008) The developmental genetics of congenital heart disease. Nature 451(7181):943-948 (Pubitemid 351301750)
15. Burggren WW, Keller BB (1997) Development of cardiovascular systems: molecules to organisms. Cambridge University Press, Cambridge
16. Butcher JT, Sedmera D, Guldberg RE, Markwald RR (2007) Quantitative volumetric analysis of cardiac morphogenesis assessed through micro-computed tomography. Dev Dyn 236(3):802-809 (Pubitemid 46449191)
17. Chabert S, Taber LA (2002) Intramyocardial pressure measurements in the stage 18 embryonic chick heart. Am J Physiol-Heart C 282(4):H1248-H1254 (Pubitemid 34654875)
18. Challice CE, Virágh S (1974) The architectural development of the early mammalian heart. Tissue Cell 6(3):447-462
19. Clark EB, Hu N, Rosenquist GC (1984) Effect of conotruncal constriction on aortic-mitral valve continuity in the stage 18, 21 and 24 chick embryo. Am J Cardiol 53(2):324-327 (Pubitemid 14215379)
20. Clark EB, Hu N, Dummett JL, Vandekieft GK, Olson C, Tomanek R (1986) Ventricular function and morphology in chick embryo from stages 18 to 29. Am J Physiol 250(3 Pt 2):H407-H413
21. 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 257(1 Pt 2):H55-H61
22. Cohn AE (1928) Physiological ontogeny: a chicken embryos. xiii. the temperature characteristic for the contraction rate of the whole heart. J Gen Physiol 11(4):369-375
23. Colvee E, Hurle JM (1983) Malformations of the semilunar valves produced in chick embryos by mechanical interference with cardiogenesis. an experimental approach to the role of hemodynamics in valvular development. Anat Embryol (Berl) 168(1):59-71 (Pubitemid 13003700)
24. Crozier WJ, Stier TJ (1927) Temperature and frequency of cardiac contractions in embryos of limulus. J Gen Physiol 10(4):501-518
25. Cuneo B, Hughes S, Benson JDW (1993) Heart rate perturbation in the stage 17-27 chick embryo: effect on stroke volume and aortic flow. Am J Physiol 264(3 Pt 2):H755-H759 (Pubitemid 23109865)
26. Damon BJ, Rémond MC, Bigelow MR, Trusk TC, Xie W, Perucchio R, Sedmera D, Denslow S, Thompson RP (2009) Patterns of muscular strain in the embryonic heartwall. Dev Dyn 238(6):1535-1546
27. de Almeida 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(9):1363-1370 (Pubitemid 46745187)
28. de Jong F, Opthof T, Wilde AA, Janse MJ, Charles R, Lamers WH, Moorman AF (1992) Persisting zones of slow impulse conduction in developing chicken hearts. Circ Res 71(2):240-250
29. DeGroff C, Thornburg B, Pentecost J, Thornburg K, Gharib M, Sahn D (2003) Flow in the early embryonic human heart: a numerical study. Pediatr Cardiol 24(4):375-380 (Pubitemid 37021438)
30. Egorova A, DeRuiter M, de Boer H, van de Pas S, Gittenberger-de Groot A, van Zonneveld A, Poelmann R, Hierck B (2011) Endothelial colony-forming cells show a mature transcriptional response to shear stress. In Vitro Cell Dev B 48(1):21-29
31. Ettensohn CA (1985) Mechanisms of epithelial invagination. Q Rev Biol 60(3):289-307
32. Faber JJ, Green TJ, Thornburg KL (1974) Embryonic stroke volume and cardiac output in the chick. Dev Biol 41(1):14-21
33. Forouhar AS, Liebling M, Hickerson A, Nasiraei-Moghaddam A, Tsai HJ, Hove JR, Fraser SE, Dickinson ME, Gharib M (2006) The embryonic vertebrate heart tube is a dynamic suction pump. Science 312(5774):751-753
34. Fransen M, Lemanski L (1988) Myocardial cell relationship during morphogenesis in normal and cardiac lethal mutant axolotls, ambystoma mexicanum. Am J Anat 183:245-257
35. Friedman S, Murphy L, Ash R (1951) Aortic atresia with hypoplasia of the left heart and aortic arch. J Pediatr 38(3):354-368
36. Fujimoto J (2003) Optical coherence tomography for ultrahigh resolution in vivo imaging. Nat Biotechnol 21:1361-1367 (Pubitemid 37356623)
37. Garita B, Jenkins MW, Han M, Zhou C, Vanauker M, Rollins AM, Watanabe M, Fujimoto JG, Linask KK (2011) Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping. Am J Physiol Heart C 300(3):H879-H891
38. Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, Klein R, Lemke G (1995) Aberrant neural and cardiac development in mice lacking the erbb4 neuregulin receptor. Nature 378(6555):390-394
39. Glaser O (1929) Temperature and heart rate in fundulus embryo. J Exp Biol 6:325-339
40. Goda T, Abu-Daya A, Carruthers S, Clark MD, Stemple DL, Zimmerman LB (2006) Genetic screens for mutations affecting development of Xenopus tropicalis. PLoS Genet 2(6):e91
41. Goodwin RL, Nesbitt T, Price RL, Wells JC, Yost MJ, Potts JD (2005) Three-dimensional model system of valvulogenesis. Dev Dyn 233(1):122-129 (Pubitemid 40548030)
42. Groenendijk B, Van der Heiden K, Hierck B, Poelmann R (2007) 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. Physiology 22:380-389
43. Grossman TR, Gamliel A, Wessells RJ, Taghli-Lamallem O, Jepsen K, Ocorr K, Korenberg JR, Peterson KL, Rosenfeld MG, Bodmer R, Bier E (2011) Over-expression of dscam and col6a2 cooperatively generates congenital heart defects. PLoS Genet 7(11): e1002344
44. Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 195(4):231-272
45. Harh J, Paul M, Gallen W, Friedberg D, Kaplan S (1973) Experimental production of hypoplastic left heart syndrome in the chick embryo. Am J Cardiol 31(1):51-56
46. 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(8):1949-1957
47. Hickerson A, Rinderknecht D, Gharib M (2005) Experimental study of the behavior of a valveless impedance pump. Exp Fluids 39(4):787-787, 0723-4864
48. Hickerson AI, Gharib M (2006) On the resonance of a pliant tube as a mechanism for valveless pumping. J Fluid Mech 555-1:141-148 (Pubitemid 44508866)
49. Hierck BP, Van der Heiden K, Poelma C, Westerweel J, Poelmann RE (2008) Fluid shear stress and inner curvature remodeling of the embryonic heart. Choosing the right lane! Sci World J 8:212-222 (Pubitemid 351317533)
50. Hochel J, Akiyama R, Masuko T, Pearson JT, Nichelmann M, Tazawa H (1998) Development of heart rate irregularities in chick embryos. Am J Physiol 275(2 Pt 2):H527-H533
51. 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(4):473-481 (Pubitemid 27137283)
52. 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(1):87-99 (Pubitemid 29016048)
53. Hou PC, Burggren WW (1995) Cardiac output and peripheral resistance during larval development in the anuran amphibian xenopus laevis. Am J Physiol 269(5 Pt 2):R1126-R1132 (Pubitemid 3005999)
54. Hove J (2006) Quantifying cardiovascular flow dynamics during early development. Pediatr Res 60(1):6-13 (Pubitemid 44297604)
55. Hove JR, Köster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M (2003) Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421(6919):172-177 (Pubitemid 36090985)
56. Hu N, Clark EB (1989) Hemodynamics of the stage 12 to stage 29 chick embryo. Circ Res 65(6):1665-1670 (Pubitemid 20023559)
57. Hu N, Keller BB (1995) Relationship of simultaneous atrial and ventricular pressures in stage 16-27 chick embryos. Am J Physiol 269(4 Pt 2):H1359-H1362
58. Hu N, Connuck DM, Keller BB, Clark EB (1991) Diastolic filling characteristics in the stage 12 to 27 chick embryo ventricle. Pediatr Res 29(4 Pt 1):334-337
59. Hu N, Sedmera D, Yost HJ, Clark EB (2000) Structure and function of the developing zebrafish heart. Anat Rec 260(2):148-157
60. Icardo J, Fernandez-Teran A (1987) Morphologic study of ventricular trabeculation in the embryonic chick heart. Acta Anat 130(3):264-274
61. Ishiwata T, Nakazawa M, Pu WT, Tevosian SG, Izumo S (2003) Developmental changes in ventricular diastolic function correlate with changes in ventricular myoarchitecture in normal mouse embryos. Circ Res 93(9):857-865 (Pubitemid 37363060)
62. Itasaki N, Nakamura H, Sumida H, Yasuda M (1991) Actin bundles on the right side in the caudal part of the heart tube play a role in dextro-looping in the embryonic chick heart. Anat Embryol (Berl) 183(1):29-39
63. Jacob E, Drexel M, Schwerte T, Pelster B (2002) Influence of hypoxia and of hypoxemia on the development of cardiac activity in zebrafish larvae. Am J Physiol-Reg I 283(4):R911-R917
64. Jenkins M, Adler D, Gargesha M, Huber R, Rothenberg F, Belding J, Watanabe M, Wilson D, Fujimoto J, Rollins A (2007) Ultrahighspeed optical coherence tomography imaging and visualization of the embryonic avian heart using a buffered fourier domain mode locked laser. Opt Express 15:6251-6267 (Pubitemid 46752918)
65. Jenkins M, Chughtai O, Basavanhally A, Watanabe M, Rollins A (2007b) In vivo imaging of the embryonic heart using gated optical coherence tomography. J Biomed Opt 12:030505
66. Jenkins M, Watanabe M, Rollins A (2012) Longitudinal imaging of heart development with optical coherence tomography. IEEE J Sel Top Quant Electron 18(3):1166-1175
67. Jones E, Baron M, Fraser S, Dickinson M (2004) Measuring hemodynamic changes during mammalian development. Am J Physiol Heart C 287(4):H1561-H1569 (Pubitemid 39313260)
68. Jung E (2007) A mathematical model of valveless pumping: a lumped model with time-dependent compliance, resistance, and inertia. Bull Math Biol 69(7):2181-2198 (Pubitemid 47415549)
69. Jung E, Peskin CS (2001) Two-dimensional simulations of valveless pumping using the immersed boundary method. SIAM J Sci Comput 23(1):19-45
70. Kamino K, Hirota A, Fujii S (1981) Localization of pacemaking activity in early embryonic heartmonitored using voltage-sensitive dye. Nature 290(5807):595-597 (Pubitemid 11092371)
71. Keller BB (1998) Embryonic cardiovascular function, coupling and maturation: a species view. In: Burggren W, Keller B (eds) Development of cardiovascular systems. University Press, Cambridge
72. Keller BB, Hu N, Clark EB (1990) Correlation of ventricular area, perimeter, and conotruncal diameter with ventricular mass and function in the chick embryo from stages 12 to 24. Circ Res 66(1):109-114 (Pubitemid 20033931)
73. Keller BB, Hu N, Serrino PJ, Clark EB (1991) Ventricular pressure-area loop characteristics in the stage 16 to 24 chick embryo. Circ Res 68(1):226-231
74. Keller BB, Tinney JP, Hu N (1994) Embryonic ventricular diastolic and systolic pressure-volume relations. Cardiol Young 4(01):19-27
75. Keller BB, MacLennan MJ, Tinney JP, Yoshigi M (1996) In vivo assessment of embryonic cardiovascular dimensions and function in day- 10.5 to -14.5 mouse embryos. Circ Res 79(2):247-255 (Pubitemid 26255876)
76. Kenner T, Moser M, Tanev I, Ono K (2000) The liebau-effect or on the optimal use of energy for the circulation of blood. Scripta Medica 73(1):9-14
77. Kilner PJ (2005) Valveless pump models that laid a false but fortuitous trail on the way towards the total cavopulmonary connection. Cardiol Young 15(Supplement S3):74-79 (Pubitemid 41601341)
78. Kim JS, Min J, Recknagel AK, Riccio M, Butcher JT (2011) Quantitative three-dimensional analysis of embryonic chick morphogenesis via microcomputed tomography. Anat Rec (Hoboken) 294(1):1-10
79. Kirchhoff S, Kim JS, Hagendorff A, Thönnissen E, Krüger O, Lamers WH, Willecke K (2000) Abnormal cardiac conduction and morphogenesis in connexin40 and connexin43 double-deficient mice. Circ Res 87(5):399-405
80. Kowalski W, Teslovich N, Dur O, Keller B, Pekkan K (2012) Computational hemodynamic optimization predicts dominant aortic arch selection is driven by embryonic outflow tract orientation in the chick embryo. Biomech Model Mechanobiol [Epub ahead of print]
81. Kunz P, Crelier GR, Schwizer W, Borovicka J, Kreiss C, Fried M, Boesiger P (1998) Gastric emptying and motility: assessment with mr imaging-preliminary observations. Radiology 207(1): 33-40 (Pubitemid 28168664)
82. Lakkis MM, Epstein JA (1998) Neurofibromin modulation of ras activity is required for normal endocardial-mesenchymal transformation in the developing heart. Development 125(22):4359-4367 (Pubitemid 28564281)
83. Lamers W, Moorman A (2002) Cardiac septation: a late contribution of the embryonic primary myocardium to heart morphogenesis. Circ Res 91:93-103 (Pubitemid 34827219)
84. Latacha KS, Rémond MC, Ramasubramanian A, Chen AY, Elson EL, Taber LA (2005) Role of actin polymerization in bending of the early heart tube. Dev Dyn 233(4):1272-1286 (Pubitemid 40995125)
85. Lee K, Simon H, Chen H, Bates B, Hung M, Hauser C (1995) Requirement for neuregulin receptor erbb2 in neural and cardiac development. Nature 378(6555):394-398
86. Liebau G (1954) Uber ein ventilloses pumpprinzip. Z Kreislaufforsch 41(14):327-328
87. Liebau G (1957) Significance of forces of inertia in the dynamics of blood circulation. Z Kreislaufforsch 46(11-12):428-438
88. Lin IE, Taber LA (1995) A model for stress-induced growth in the developing heart. J Biomech Eng 117:343-349
89. Lincoln J, Alfieri CM, Yutzey KE (2004) Development of heart valve leaflets and supporting apparatus in chicken and mouse embryos. Dev Dyn 230(2):239-250 (Pubitemid 38669586)
90. Ling P, Taber L, Humphrey J (2002) Approach to quantify the mechanical behavior of the intact embryonic chick heart. Ann Biomed Eng 30:636-645 (Pubitemid 34783431)
91. Liu A, Nickerson A, Troyer A, Yin X, Cary R, Thornburg K, Wang R, Rugonyi S (2011) Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts. Comput Struct 89(11-12):855-867
92. Loots E, Hillen B, Veldman AEP (2003) The role of hemodynamics in the development of the outflow tract of the heart. J Eng Math 45(1):91-104, 0022-0833 (Pubitemid 36352524)
93. Loumes L, Avrahami I, Gharib M (2008) Resonant pumping in a multilayer impedance pump. Phys Fluids 20(2):023-103
94. Lucitti JL, Tobita K, Keller BB (2005) Arterial hemodynamics and mechanical properties after circulatory intervention in the chick embryo. J Exp Biol 208(Pt 10):1877-1885 (Pubitemid 40817097)
95. Ma L, Lu MF, Schwartz RJ, Martin JF (2005) Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition andmyocardial patterning. Development 132(24):5601-5611 (Pubitemid 43125885)
96. Ma Z, Liu A, Yin X, Troyer A, Wang R, Rugonyi S (2010) Absolute flow velocity measurement in hh18 chicken embryo outflow tract based on 4d reconstruction using spectral domain optical coherence tomography. Biomed Opt Express 1:798-811
97. Männer J (2000) Cardiac looping in the chick embryo: amorphological review with special reference to terminological and biomechanical aspects of the looping process. Anat Rec 259(3):248-262 (Pubitemid 30445885)
98. Männer J (2004) On rotation, torsion, lateralization, and handedness of the embryonic heart loop: new insights from a simulation model for the heart loop of chick embryos. Anat Rec A Discov Mol Cell Evol Biol 278(1):481-492 (Pubitemid 38619661)
99. Manner J, Thrane L, Norozi K, Yelbuz T (2008) High-resolution in vivo imaging of the cross-sectional deformations of contracting embryonic heart loops using optical coherence tomography. Dev Dyn 237(4):953-961 (Pubitemid 351542293)
100. Manner J, Thrane L, Norozi K, Yelbuz T (2009) In vivo imaging of the cyclic changes in cross-sectional shape of the ventricular segment of pulsating embryonic chick hearts at stages 14 to 17: a contribution to the understanding of the ontogenesis of cardiac pumping function. Dev Dyn 238(12):3273-3278
101. Manner J, Wessel A, Yelbuz TM (2010) How does the tubular embryonic heart work? Looking for the physical mechanism generating unidirectional blood flow in the valveless embryonic heart tube. Dev Dyn 239(4):1035-1046
102. Maron BJ, Hutchins GM (1974) The development of the semilunar valves in the human heart. Am J Pathol 74(2):331-344
103. Martinsen BJ (2005) Reference guide to the stages of chick heart embryology. Dev Dyn 233(4):1217-1237 (Pubitemid 40995121)
104. Mercola M, Levin M (2001) Left-right asymmetry determination in vertebrates. Annu Rev Cell Dev Biol 17:779-805 (Pubitemid 33096191)
105. Meyer D, Birchmeier C (1995) Multiple essential functions of neuregulin in development. Nature 378(6555):386-390
106. Miller CE, Wong CL, Sedmera D (2003) Pressure overload alters stressstrain properties of the developing chick heart. Am J Physiol Heart C 285(5):H1849-H1856 (Pubitemid 37305924)
107. Miura GI, Yelon D (2011) A guide to analysis of cardiac phenotypes in the zebrafish embryo. Methods Cell Biol 101:161-180
108. Moser M, Huang JW, Schwarz GS, Kenner T, Noordergraaf A (1998) Impedance defined flow generalisation of william harvey's concept of the circulation - 370 years later. Int J Cardiovasc Med Sci 1:205-211
109. Nomura-Kitabayashi A, Phoon CKL, Kishigami S, Rosenthal J, Yamauchi Y, Abe K, Yamamura Ki, Samtani R, Lo CW, Mishina Y (2009) Outflow tract cushions perform a critical valve-like function in the early embryonic heart requiring bmpria-mediated signaling in cardiac neural crest. Am J Physiol Heart C 297(5):H1617-H1628
110. Ong LL, Kim N, Mima T, Cohen-Gould L, Mikawa T (1998) Trabecular myocytes of the embryonic heart require n-cadherin for migratory unit identity. Dev Biol 193(1):1-9 (Pubitemid 28096576)
111. Oostra RJ, Steding G, Virágh S (2007) Steding's and Virágh's scanning electronmicroscopy atlas of the developing human heart. Springer, New York
112. O'Rahilly R, Muller F (1987) Developmental stages in human embryos. Carnegie Institution Washington Publication, Washington, DC 673
113. O'Rahilly R, Muller F (2010) Developmental stages in human embryos: revised and new measurements. Cells Tissues Organs 192(2):73-84
114. Ottesen JT (2003) Valveless pumping in a fluid-filled closed elastic tube-system: one-dimensional theory with experimental validation. J Math Biol 46(4):309-332 (Pubitemid 38355712)
115. Paff GH (1940) A micro-method for digitalis assay. J Pharmacol Exp Ther 69(4):311-315
116. Paff GH, Johnson JR (1938) The behavior of the embryonic heart in solutions of ouabain. Am J Physiol 122(3):753-758
117. Paff GH, Boucek RJ, Klopfenstein HS (1964) Experimental heart-block in the chick embryo. Anat Rec 149:217-223
118. Parpart ER, Glaser O (1929) Temperature and heart rate in chick embryos. J Exp Biol 7:143-153
119. Pelster B, Burggren WW (1996) Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebra fish (danio rerio). Circ Res 79(2):358-362 (Pubitemid 26259878)
120. Phelan CM, Hughes SF, Benson JDW (1995) Heart rate-dependent characteristics of diastolic ventricular filling in the developing chick embryo. Pediatr Res 37(3):289-293
121. Phoon C, Turnbull D (2003) Ultrasound biomicroscopy-doppler in mouse cardiovascular development. Physiol Genomics 14(1):3-15 (Pubitemid 37345210)
122. Phoon C, Ji R, Aristizabal O, Worrad D, Zhou B, Baldwin H, Turnbull D (2004) Embryonic heart failure in nfatc1-/- mice: novel mechanistic insights from in utero ultrasound biomicroscopy. Circ Res 95(1):92-99 (Pubitemid 38931840)
123. Poelmann R, Gittenberger-de Groot A, Hierck B (2008) The development of the heart and microcirculation: role of shear stress. Med Biol Eng Comput 46:479-484
124. Rauhut-Klaban M, Bruska M, Wózniak W (2008) Early trabeculation and closure of the interventricular foramen in staged human embryos. Folia Morphol (Warsz) 67(1):13-18 (Pubitemid 351404054)
125. Reckova M, Rosengarten C, de Almeida A, Stanley CP, Wessels A, Gourdie RG, Thompson RP, Sedmera D (2003) Hemodynamics is a key epigenetic factor in development of the cardiac conduction system. Circ Res 93(1):77-85 (Pubitemid 36859044)
126. Rodbard S (1956) Vascular modifications induced by flow. Am Heart J 51(6):926-942
127. Rodriguez EK, Hoger A, McCulloch AD (1994) Stress-dependent finite growth in soft elastic tissues. J Biomech 27(4):455-467 (Pubitemid 24102058)
128. 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(18):5077-5091
129. Rychter Z (1978) Analysis of relations between aortic arches and aorticopulmonary septation. Birth Defects Orig Artic Ser 14(7):443-448 (Pubitemid 9202612)
130. Rychter Z, Rychterova V (1981) Angio- and myoarchitecture of the heart wall under normal and experimentally changed morphogenesis. Raven Press, New York 431-452
131. Rychter Z, Rychterova V, Lemez L (1979) Formation of the heart loop and proliferation structure of its wall as a base for ventricular septation. Herz 4:86-90 (Pubitemid 9141888)
132. Rychterova V (1971) Principle of growth in thickness of the heart ventricular wall in the chick embryo. Folia Morphol (Praha) 19:262-272
133. Santhanakrishnan A, Miller L (2011) Fluid dynamics of heart development. Cell Biochem Biophys 61(1):1-22
134. Savagner P (2001) Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 23(10):912-923 (Pubitemid 32972691)
135. Sedmera D, Pexieder T, Hu N, Clark EB (1997) Developmental changes in the myocardial architecture of the chick. Anat Rec 248(3):421-432 (Pubitemid 27280149)
136. 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(2):238-252 (Pubitemid 29053228)
137. Sedmera D, Hu N, Weiss KM, Keller BB, Denslow S, Thompson RP (2002) Cellular changes in experimental left heart hypoplasia. Anat Rec 267(2):137-145 (Pubitemid 34587368)
138. Smith T, Bader D (2007) Signals from both sides: control of cardiac development by the endocardium and epicardium. Semin Cell Dev Biol 18(1):84-89 (Pubitemid 46350740)
139. Srivastava D (2006) Genetic regulation of cardiogenesis and congenital heart disease. Annu Rev Pathol 1:199-213
140. Stalsberg H (1970) Development and ultrastructure of the embryonic heart. ii. mechanism of dextral looping of the embryonic heart. Am J Cardiol 25(3):265-271
141. Stekelenburg-de Vos S, Ursem NTC, Hop WCJ, Wladimiroff JW, Gittenberger-de Groot AC, Poelmann RE (2003) Acutely altered hemodynamics following venous obstruction in the early chick embryo. J Exp Biol 206(Pt 6):1051-1057 (Pubitemid 36386403)
142. Stekelenburg-de Vos S, Steendijk P, Ursem NT, Wladimiroff JW, Delfos R, Poelmann RE (2005) Systolic and diastolic ventricular function assessed by pressure-volume loops in the stage 21 venous clipped chick embryo. Pediatr Res 57(1):16-21 (Pubitemid 40039887)
143. Taber LA (1991) On a nonlinear theory for muscle shells: part ii-application to the beating left ventricle. J Biomech Eng 113(1):63-71
144. Taber LA (1998) Mechanical aspects of cardiac development. Prog Biophys Mol Biol 69(2-3):237-255 (Pubitemid 28421468)
145. Taber LA, Humphrey J (2001) Stress-modulated growth, residual stress, and vascular heterogeneity. J Biomech Eng 123:528-535 (Pubitemid 34016544)
146. Taber LA, Lin IE, Clark EB (1995) Mechanics of cardiac looping. Dev Dyn 203(1):42-50
147. Taber LA, Zhang J, Perucchio R (2007) Computational model for the transition from peristaltic to pulsatile flow in the embryonic heart tube. J Biomech Eng 129(3):441-449 (Pubitemid 47066858)
148. Tobita K, Keller BB (2000) Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos. Am J Physiol Heart C 279(3):H959-H969
149. 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 C 282(6):H2386-H2396 (Pubitemid 34663051)
150. Tomlins P, Wang R (2005) Theory, development and applications of optical coherence tomography. J Phys D Appl Phys 38:2519-2535 (Pubitemid 41067740)
151. Ursem NTC, Stekelenburg-de Vos S, Wladimiroff JW, Poelmann RE, Gittenberger-deGroot AC, Hu N, Clark EB (2004) Ventricular diastolic filling characteristics in stage-24 chick embryos after extraembryonic venous obstruction. J Exp Biol 207(Pt 9):1487-1490 (Pubitemid 38571984)
152. Usha S, Rao AR (1995) Peristaltic transport of a biofluid in a pipe of elliptic cross section. J Biomech 28(1):45-52 (Pubitemid 24343731)
153. Van den Berg G, Moorman A (2009) Concepts of cardiac development in retrospect. Pediatr Cardiol 30:580-587
154. Van der Heiden K, Groenendijk B, Hierck B, Hogers B, Koerten H, Mommaas A, Gittenberger-de Groot A, Poelmann R (2006) Monocilia on chicken embryonic endocardium in low shear stress areas. Dev Dyn 235:19-28 (Pubitemid 46939699)
155. Vennemann P, Kiger KT, Lindken R, Groenendijk BC, Stekelenburg-de Vos S, ten Hagen TL, Ursem NT, Poelmann RE, Westerweel J, Hierck BP (2006) In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart. J Biomech 39(7):1191-1200
156. Vermot J, Forouhar A, Liebling M, Wu D, Plummer D, Gharib M, Fraser S (2009) Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol 7(11):2511-2524
157. Voronov DA, Taber LA (2002) Cardiac looping in experimental conditions: effects of extraembryonic forces. Dev Dyn 224(4):413-421 (Pubitemid 34848065)
158. Voronov DA, Alford PW, Xu G, Taber LA (2004) The role of mechanical forces in dextral rotation during cardiac looping in the chick embryo. Dev Biol 272(2):339-350 (Pubitemid 38988261)
159. Wagman AJ, Hu N, Clark EB (1990) Effect of changes in circulating blood volume on cardiac output and arterial and ventricular blood pressure in the stage 18, 24, and 29 chick embryo. Circ Res 67(1):187-192 (Pubitemid 20223739)
160. Wagner M, Siddiqui MAQ (2007) Signal transduction in early heart development (ii): ventricular chamber specification, trabeculation, and heart valve formation. Exp Biol Med (Maywood) 232(7):866-880 (Pubitemid 47026792)
161. Wang Y, Dur O, Patrick MJ, Tinney JP, Tobita K, Keller BB, Pekkan K (2009) Aortic arch morphogenesis and flow modeling in the chick embryo. Ann Biomed Eng 37(6):1069-1081
162. Warkman AS, Krieg PA (2007) Xenopus as a model system for vertebrate heart development. Semin Cell Dev Biol 18(1):46-53 (Pubitemid 46330842)
163. Yalcin HC, Shekhar A, Nishimura N, Rane AA, Schaffer CB, Butcher JT (2010) Two-photon microscopy-guided femtosecondlaser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects. Am J Physiol Heart C 299(5):H1728-H1735
164. Yalcin HC, Shekhar A, McQuinn TC, Butcher JT (2011) Hemodynamic patterning of the avian atrioventricular valve. Dev Dyn 240(1):23-35
165. Yang M, Taber LA, Clark EB (1994) A nonlinear poroelastic model for the trabecular embryonic heart. J Biomech Eng 116(2):213-223 (Pubitemid 24177120)
166. Yoshigi M, Keller B (1997) Characterization of embryonic aortic impedance with lumped parameter models. Am J Physiol Heart C 42(1):H19-H27
167. Zhou YQ, Foster FS, Qu DW, Zhang M, Harasiewicz KA, Adamson SL (2002) Applications for multifrequency ultrasound biomicroscopy in mice from implantation to adulthood. Physiol Genomics 10(2):113-126 (Pubitemid 135707435)