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

The cardiac cycle‐related deformations of tubular embryonic hearts were traditionally described as concentric narrowing and widening of a tube of circular cross‐section. Using optical coherence tomography (OCT), we have recently shown that, during the cardiac cycle, only the myocardial tube undergoes concentric narrowing and widening while the endocardial tube undergoes eccentric narrowing and widening, having an elliptic cross‐section at end‐diastole and a slit‐shaped cross‐section at end‐systole. Due to technical limitations, these analyses were confined to early stages of ventricular development (chick embryos, stages 10–13). Using a modified OCT‐system, we now document, for the first time, the cyclic changes in cross‐sectional shape of beating embryonic ventricles at stages 14 to 17. We show that during these stages (1) a large area of diminished cardiac jelly appears at the outer curvature of the ventricular region associated with formation of endocardial pouches; (2) the ventricular endocardial lumen acquires a bell‐shaped cross‐section at end‐diastole and becomes compressed like a fireplace bellows during systole; (3) the contracting portions of the embryonic ventricles display stretching along its baso‐apical axis at end‐systole. The functional significance of our data is discussed with respect to early cardiac pumping function. Developmental Dynamics 238:3273–3284, 2009. © 2009 Wiley‐Liss, Inc.

[1]  David L Wilson,et al.  High temporal resolution OCT using image-based retrospective gating. , 2009, Optics express.

[2]  Renato Perucchio,et al.  Patterns of muscular strain in the embryonic heart wall , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[3]  J. Duker,et al.  Ultrahigh Speed Optical Coherence Tomography Imaging of Human Retina Using Swept Source / Fourier Domain OCT , 2009 .

[4]  Joseph Izatt,et al.  Quantitative Measurement of Blood Flow Dynamics in Embryonic Vasculature Using Spectral Doppler Velocimetry , 2009, Anatomical record.

[5]  Jakob Thomsen,et al.  Field programmable gate-array-based real-time optical Doppler tomography system for in vivo imaging of cardiac dynamics in the chick embryo , 2009 .

[6]  A. Moorman,et al.  Can recent insights into cardiac development improve our understanding of congenitally malformed hearts? , 2009, Clinical anatomy.

[7]  J. Männer The anatomy of cardiac looping: A step towards the understanding of the morphogenesis of several forms of congenital cardiac malformations , 2009, Clinical anatomy.

[8]  J. Izatt,et al.  In vivo spectral domain optical coherence tomography volumetric imaging and spectral Doppler velocimetry of early stage embryonic chicken heart development. , 2008, Journal of the Optical Society of America. A, Optics, image science, and vision.

[9]  Ruikang K. Wang,et al.  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 , 2008, Physics in medicine and biology.

[10]  Jörg Männer,et al.  High‐resolution in vivo imaging of the cross‐sectional deformations of contracting embryonic heart loops using optical coherence tomography , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[11]  T M Yelbuz,et al.  In vivo visualisation of coronary artery development by high-resolution optical coherence tomography , 2008, Heart.

[12]  David Sedmera,et al.  High‐frequency ultrasonographic imaging of avian cardiovascular development , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[13]  Renato Perucchio,et al.  Computational model for the transition from peristaltic to pulsatile flow in the embryonic heart tube. , 2007, Journal of biomechanical engineering.

[14]  Roger R Markwald,et al.  Transitions in Early Embryonic Atrioventricular Valvular Function Correspond With Changes in Cushion Biomechanics That Are Predictable by Tissue Composition , 2007, Circulation research.

[15]  Michael W. Jenkins,et al.  Ultrahigh-speed optical coherence tomography imaging and visualization of the embryonic avian heart using a buffered Fourier Domain Mode Locked laser. , 2007, Optics express.

[16]  Jörg Männer,et al.  Construction and Establishment of a New Environmental Chamber to Study Real-Time Cardiac Development , 2007, Microscopy and Microanalysis.

[17]  J. Xavier-Neto,et al.  Parallel avenues in the evolution of hearts and pumping organs. , 2007, Cellular and molecular life sciences : CMLS.

[18]  J. Xavier-Neto,et al.  Cardiovascular development: towards biomedical applicability , 2007, Cellular and Molecular Life Sciences.

[19]  Michael W. Jenkins,et al.  Phenotyping transgenic embryonic murine hearts using optical coherence tomography. , 2006, Applied optics.

[20]  Michael Liebling,et al.  Rapid three‐dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[21]  Jan M. Ruijter,et al.  Regionalized Sequence of Myocardial Cell Growth and Proliferation Characterizes Early Chamber Formation , 2006, Circulation research.

[22]  Anna I Hickerson,et al.  The Embryonic Vertebrate Heart Tube Is a Dynamic Suction Pump , 2006, Science.

[23]  Daniel L Marks,et al.  Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system. , 2006, Journal of biomedical optics.

[24]  A. Wessels,et al.  Elevated vascular endothelial cell growth factor affects mesocardial morphogenesis and inhibits normal heart bending , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[25]  Jörg Männer,et al.  On rotation, torsion, lateralization, and handedness of the embryonic heart loop: new insights from a simulation model for the heart loop of chick embryos. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[26]  G. Steding,et al.  Experimental study on the significance of abnormal cardiac looping for the development of cardiovascular anomalies in neural crest-ablated chick embryos , 1996, Anatomy and Embryology.

[27]  Joseph A. Izatt,et al.  Optical Coherence Tomography: A New High-Resolution Imaging Technology to Study Cardiac Development in Chick Embryos , 2002, Circulation.

[28]  Renato Perucchio,et al.  Modeling Heart Development , 2000 .

[29]  Jörg Männer,et al.  Cardiac looping in the chick embryo: A morphological review with special reference to terminological and biomechanical aspects of the looping process , 2000, The Anatomical record.

[30]  Robert H. Anderson,et al.  Developmental patterning of the myocardium , 2000, The Anatomical record.

[31]  D G Gibson,et al.  Normal long axis function , 1999, Heart.

[32]  E. Clark,et al.  Developmental changes in the myocardial architecture of the chick , 1997, The Anatomical record.

[33]  J. Fujimoto,et al.  Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomography. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Usha,et al.  Peristaltic transport of a biofluid in a pipe of elliptic cross section. , 1995, Journal of biomechanics.

[35]  C. Coulam,et al.  Very early (24-56 days from last menstrual period) embryonic heart rate in normal pregnancies. , 1994, Human reproduction.

[36]  J. Wisser,et al.  Embryonic heart rate in dated human embryos. , 1994, Early human development.

[37]  Bradley B Keller,et al.  Diastolic Filling Characteristics in the Stage 12 to 27 Chick Embryo Ventricle , 1991, Pediatric Research.

[38]  N. Hu,et al.  Hemodynamics of the Stage 12 to Stage 29 Chick Embryo , 1989, Circulation research.

[39]  J. Icardo,et al.  Morphologic study of ventricular trabeculation in the embryonic chick heart. , 1987, Acta anatomica.

[40]  A. Nakamura Cardiac hyaluronidase activity of chick embryos at the time of endocardial cushion formation. , 1980, Journal of molecular and cellular cardiology.

[41]  J. Hurlé,et al.  Compositional and structural heterogenicity of the cardiac jelly of the chick embryo tubular heart: a TEM, SEM and histochemical study. , 1980, Journal of embryology and experimental morphology.

[42]  F. Manasek,et al.  Experimental studies of the shape and structure of isolated cardiac jelly. , 1978, Journal of embryology and experimental morphology.

[43]  T. Pexieder Development of the outflow tract of the embryonic heart. , 1978, Birth defects original article series.

[44]  F. Manasek,et al.  Cardiac jelly fibrils: their distribution and organization. , 1978, Birth defects original article series.

[45]  I. Gessner,et al.  Acid mucopolysaccharide content of the cardiac jelly of the chick embryo. , 1965, The Journal of experimental zoology.

[46]  Viktor Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1992, Journal of morphology.

[47]  A. Barry,et al.  The functional significance of the cardiac jelly in the tubular heart of the chick embryo , 1948 .

[48]  C. M. Goss THE PHYSIOLOGY OF THE EMBRYONIC MAMMALIAN HEART BEFORE CIRCULATION , 1942 .

[49]  B. M. Patten,et al.  The initiation of contraction in the embryonic chick heart , 1933 .