Abstract
.Significance: Understanding how the valveless embryonic heart pumps blood is essential to elucidate biomechanical cues regulating cardiogenesis, which is important for the advancement of congenital heart defects research. However, methods capable of embryonic cardiac pumping analysis remain limited, and assessing this highly dynamic process in mammalian embryos is challenging. New approaches are critically needed to address this hurdle.Aim: We report an imaging-based approach for functional assessment of localized pumping dynamics in the early tubular embryonic mouse heart.Approach: Four-dimensional optical coherence tomography was used to obtain structural and Doppler hemodynamic imaging of the beating heart in live mouse embryos at embryonic day 9.25. The pumping assessment was performed based on the volumetric blood flow rate, flow resistance within the heart tube, and pressure gradient induced by heart wall movements. The relation between the blood flow, the pressure gradient, and the resistance to flow were evaluated through temporal analyses and Granger causality test.Results: In the ventricles, our method revealed connections between the temporal profiles of pressure gradient and volumetric blood flow rate. Statistically significant causal relation from the pressure gradient to the blood flow was demonstrated. Our analysis also suggests that cardiac pumping in the early ventricles is a combination of suction and pushing. In contrast, in the outflow tract, where the conduction wave is slower than the blood flow, we did not find significant causal relation from pressure to flow, suggesting that, different from ventricular regions, the local active contraction of the outflow tract is unlikely to drive the flow in that region.Conclusions: We present an imaging-based approach that enables localized assessment of pumping dynamics in the mouse tubular embryonic heart. This method creates a new opportunity for functional analysis of the pumping mechanism underlying the developing mammalian heart at early stages and could be useful for studying biomechanical changes in mutant embryonic hearts that model congenital heart defects.
Highlights
How a valveless embryonic heart tube pumps blood has been a long-standing question.[1]
Our analysis suggests that cardiac pumping in the early ventricles is a combination of suction and pushing
This method creates a new opportunity for functional analysis of the pumping mechanism underlying the developing mammalian heart at early stages and could be useful for studying biomechanical changes in mutant embryonic hearts that model congenital heart defects
Summary
How a valveless embryonic heart tube pumps blood has been a long-standing question.[1] Early observations led to the traditional view that the tubular heart functions with peristaltic waves pushing the blood through the heart for circulation.[2,3] hemodynamic data in recent decades described features of blood flow that could not be explained by the classic peristaltic. Pumping model.[4,5] Notably, one study on zebrafish embryos showed that the valveless heart does not drive blood circulations through peristalsis, but rather through a suction mechanism.[6] Such suction-like pumping was observed in chick embryos.[7] The complexity of the tubular heart pumping dynamics was emphasized in a review by Männer et al.[1] about a decade ago, indicating that further functional analyses are needed to elucidate how the early embryonic heart works. Studies have mainly focused on avian and teleost models,[4,5,6,7] leaving the cardiac pumping mechanism in mammalian embryos largely unexplored
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