The Driving Mechanism for Unidirectional Blood Flow in the Tubular Embryonic Heart
- 423 Downloads
The embryonic heart of vertebrate embryos, including humans, has a tubular thick-wall structure when it first starts to beat. The tubular embryonic heart (TEH) does not have valves, and yet, it produces an effective unidirectional blood flow. The actual pumping mechanism of the TEH is still controversial with pros and cons for either peristaltic pumping (PP) or impedance pumping (IP). On the other hand, observation of movies of the contractile TEH of the quail revealed a propagating wave from the venous end towards the arterial end that occludes the lumen behind the leading edge. This pattern of contraction represents a complex PP with a duty cycle, and was defined here as biological pumping (BP). In this work we developed a heart-like model that represents the main features of the chick TEH and allows for numerical analysis of all the three pumping mechanisms (i.e., IP, PP, and BP) as well as a comprehensive sensitivity evaluation of the structural, operating, and mechanical parameters. The physical model also included components representing the whole circulatory system of the TEH. The simulations results revealed that the BP mechanism yielded the level and time-dependent pattern of blood flow and blood pressure, as well as contractility that were observed in experiments.
KeywordsEmbryonic heart Impedance pumping Valveless pumping Peristaltic pumping Fluid–Structure Interaction
Conflict of Interests
Video S1. Variation of normalized functions that represent the TEH contraction for the reference case for IP, PP, and BP mechanisms in space and time. The video is 1/5 of the original speed. Supplementary material 1 (WMV 662 kb).
Video S2. The calculated deformation of the TEH wall and blood velocity vectors for the reference cases for the IP, PP, and BP mechanisms. The video is 1/5 of the original speed. Supplementary material 2 (WMV 2771 kb).
Video S3. The calculated deformations of lumen heart-wall interface of the TEH for the reference case for IP, PP, and BP mechanisms and of motion of lumen heart-wall interface of HH-10 quail TEH traced from published videos (Jenkins et al., 2007). Supplementary material 3 (WMV 1692 kb).
- 1.Adina R&D Inc. ADINA theory and modeling guides: Adina CFD & FSI. Report ARD 13-10, 2013.Google Scholar
- 7.Chi, N. C., R. M. Shaw, B. Jungblut, J. Huisken, T. Ferrer, R. Arnaout, I. Scott, D. Beis, T. Xiao, H. Baier, L. Y. Jan, M. Tristani-Firouzi, and D. Y. R. Stainier. Genetic and physiologic dissection of the vertebrate cardiac conduction system. PLoS Biol. 6:e109, 2008.CrossRefPubMedPubMedCentralGoogle Scholar
- 12.Groenendijk, B. C. W., B. P. Hierck, J. Vrolijk, M. Baiker, M. J. B. M. Pourquie, A. C. Gittenberger-de Groot, and R. E. Poelmann. Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo. Circ. Res. 96:1291–1298, 2005.CrossRefPubMedGoogle Scholar
- 14.Heebøll-Christensen, J. Mathematical modeling of flow characteristics in the embryonic chick heart, 2011.Google Scholar
- 18.Jenkins, M. W., D. C. Adler, M. Gargesha, R. Huber, F. Rothenberg, J. Belding, M. Watanabe, D. L. Wilson, J. G. Fujimoto, and A. M. Rollins. Ultrahigh-speed optical coherence tomography imaging and visualization of the embryonic avian heart using a buffered Fourier domain mode locked laser. Opt. Exp. 15:6251–6267, 2007.CrossRefGoogle Scholar
- 22.Latacha, K. S., M. C. Rémond, A. Ramasubramanian, A. Y. Chen, E. L. Elson, and L. A. Taber. Role of actin polymerization in bending of the early heart tube. Dev. Dyn. Off. Publ. Am. Assoc. Anat. 233:1272–1286, 2005.Google Scholar
- 23.Lee, J., M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai. Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis. PLoS One 8:e72924, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
- 30.Männer, J., L. Thrane, K. Norozi, and T. M. Yelbuz. 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. Off. Publ. Am. Assoc. Anat. 238:3273–3284, 2009.Google Scholar
- 31.Männer, J., A. Wessel, and T. M. Yelbuz. How does the tubular embryonic heart work? Looking for the physical mechanism generating unidirectional blood flow in the valveless embryonic heart tube. Dev. Dyn. Off. Publ. Am. Assoc. Anat. 239:1035–1046, 2010.Google Scholar
- 35.Meier, G. Viscous Flow in the Embryonic Heart Geometry. Embryol. Hefte 1:1–19, 1987.Google Scholar
- 38.Rideout, V. C. Mathematical and Computer Modeling of Physiological Systems. Englewood Cliffs: Prentice Hall, 1991.Google Scholar
- 40.Rugonyi, S. On finite element analysis of fluid flows fully coupled with structural interactions. CMES 2:195–212, 2001.Google Scholar
- 42.Taber, L. A., and R. Perucchio. Modeling heart development. J. Elast. Phys. Sci. Solids 61:165–197, 2000.Google Scholar
- 44.Ursem, N. T. C., S. Stekelenburg-de Vos, J. W. Wladimiroff, R. E. Poelmann, A. C. Gittenberger-de Groot, N. Hu, and E. B. Clark. Ventricular diastolic filling characteristics in stage-24 chick embryos after extra-embryonic venous obstruction. J. Exp. Biol. 207:1487–1490, 2004.CrossRefPubMedGoogle Scholar
- 45.Waldrop, L., and L. Miller. Large amplitude, short wave peristalsis and its implications for transport, 2015. doi: 10.7287/peerj.preprints.906v1.