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.

The Chicken as a Model Organism to Study Heart Development

“…Optical coherence tomography and ultrasound imaging of avian embryos were used together with modeling to determine the pumping mechanisms that lead to pulsating blood flow. This implicated both peristaltic and impedance pumping mechanisms (Butcher et al 2007;Kozlovsky et al 2016). Better understanding of the biomechanics underlying blood flow has important clinical implications, for example, for surgery after aortic dissection or myocardial infarct (for review, see Furst 2015).…”

Net flow generation in closed-loop valveless pumping

“…12 showed through high-speed confocal imaging that the primitive heart tube operates like an impedance pump, whereas Kozlovsky et al. 13,14 employing one as well as three-dimensional flow models examined in detail the chick embryonic heart behavior.…”

Uncertainty quantification reveals the physical constraints on pumping by peristaltic hearts

“…There is some debate as to whether the pumping mechanisms of tubular, valveless hearts in animals best fits with the definition of peristalsis or Liebau pumping (for recent discussions, see [31,33]). Recent work has suggested that peristalsis or some peristalsis-like mechanism bests fits the available data and theoretical understanding of each mechanism [32,[34][35][36]. Here, we simplify the situation by focusing exclusively on peristaltic pumping by tubular hearts.…”