The Driving Mechanism for Unidirectional Blood Flow in the Tubular Embryonic Heart

Abstract

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.

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Correspondence to Pavel Kozlovsky.

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Associate Editor Jane Grande-Allen oversaw the review of this article.

Electronic supplementary material

Below is the link to the electronic supplementary material.

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).

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Kozlovsky, P., Bryson-Richardson, R.J., Jaffa, A.J. et al. The Driving Mechanism for Unidirectional Blood Flow in the Tubular Embryonic Heart. Ann Biomed Eng 44, 3069–3083 (2016). https://doi.org/10.1007/s10439-016-1620-8

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Keywords

  • Embryonic heart
  • Impedance pumping
  • Valveless pumping
  • Peristaltic pumping
  • Fluid–Structure Interaction