The Embryonic Vertebrate Heart Tube Is a Dynamic Suction Pump

Abstract

The embryonic vertebrate heart begins pumping blood long before the development of discernable chambers and valves. At these early stages, the heart tube has been described as a peristaltic pump. Recent advances in confocal laser scanning microscopy and four-dimensional visualization have warranted another look at early cardiac structure and function. We examined the movement of cells in the embryonic zebrafish heart tube and the flow of blood through the heart and obtained results that contradict peristalsis as a pumping mechanism in the embryonic heart. We propose a more likely explanation of early cardiac dynamics in which the pumping action results from suction due to elastic wave propagation in the heart tube.

Rapid three‐dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development

“…3A,B, Supplementary Movies 1 and 2; n ϭ 10). In parallel studies, we have explored the nature of this pumping and found that it is not due to peristalsis but, instead, results from the impedance mismatches that are present between the inflow tract, the outflow tract, and the heart tube, creating a suction pump (Forouhar et al, 2006). By 33 hpf, heart looping has begun (Fig.…”

“…Our previous studies have also shown that even at the heart tube stage, pumping efficiency is highly sensitive to changes in heart beat frequency with temperature, suggesting that such valveless pumping may not be suitable for postembryonic circulation (Forouhar et al, 2006).…”

“…Although the quantitative and dynamic information about heart morphology and blood flow should, eventually, lead to a more complete characterization of mutants and permit a variety of tests, the analysis of normal heart dynamics exhibits previously unappreciated feature richness. The quantitative approaches that have been used in this study permit the generation of models of heart function, providing information about wall motion, muscle contraction (data not shown; see Forouhar et al, 2006), cushion and valve motion, and blood flow, depending on which transgenic fluorescent protein marker line is used. The ability to resolve 3D motion also makes it possible to quantify certain events, such as changes in volume or the speed of movement of heart wall cells; however, it is not possible to track the movements of cells if the motion is not periodic.…”

“…In its earliest stages of development, the heart tube is surprisingly efficient, moving the blood forward without valves (Forouhar et al, 2006); however, as the heart grows and loops, this ability is lost. Retrograde flow is coincident with the expansion of the heart tube to form chambers and is concurrent with an increase in the blood volume and peripheral resistance.…”

Quantitative volumetric analysis of cardiac morphogenesis assessed through micro‐computed tomography

“…The heart begins as a linear tube of myocardium lined with endocardial cells that functions like a suction pump (Forouhar et al, 2006), but quickly loops and grows into a fourchambered heart complete with valves and septa that pumps in a piston manner. This process involves several key events that happen in three dimensions, including linear heart tube looping, septation of the ventricles, and development of the atrioventricular (AV) valve apparatus, defects in which result in a myriad of clinically relevant congenital heart defects (Collins-Nakai and McLaughlin, 2002;Gittenberger-de Groot et al, 2005).…”