Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping

Author:

Garita Barbara12,Jenkins Michael W.3,Han Mingda1,Zhou Chao4,VanAuker Michael2,Rollins Andrew M.3,Watanabe Michiko5,Fujimoto J. G.4,Linask Kersti K.1

Affiliation:

1. Department of Pediatrics, The Children's Research Institute, University of South Florida and All Children's Hospital, St. Petersburg; and

2. Department of Chemical Engineering, University of South Florida, Tampa, Florida;

3. Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio;

4. Department of Electrical Engineering and Computer Science and Research Laboratory of Electronics, Massachusetts Institute of Technology, Cambridge, Massachusetts; and

5. Department of Pediatrics, Case Western Reserve University, and Rainbow Babies and Children's Hospital, Cleveland, Ohio

Abstract

Analyses of form-function relationships during heart looping are directly related to technological advances. Recent advances in four-dimensional optical coherence tomography (OCT) permit observations of cardiac dynamics at high-speed acquisition rates and high resolution. Real-time observation of the avian stage 13 looping heart reveals that interactions between the endocardial and myocardial compartments are more complex than previously depicted. Here we applied four-dimensional OCT to elucidate the relationships of the endocardium, myocardium, and cardiac jelly compartments in a single cardiac cycle during looping. Six cardiac levels along the longitudinal heart tube were each analyzed at 15 time points from diastole to systole. Using image analyses, the organization of mechanotransducing molecules, fibronectin, tenascin C, α-tubulin, and nonmuscle myosin II was correlated with specific cardiac regions defined by OCT data. Optical coherence microscopy helped to visualize details of cardiac architectural development in the embryonic mouse heart. Throughout the cardiac cycle, the endocardium was consistently oriented between the midline of the ventral floor of the foregut and the outer curvature of the myocardial wall, with multiple endocardial folds allowing high-volume capacities during filling. The cardiac area fractional shortening is much higher than previously published. The in vivo profile captured by OCT revealed an interaction of the looping heart with the extra-embryonic splanchnopleural membrane providing outside-in information. In summary, the combined dynamic and imaging data show the developing structural capacity to accommodate increasing flow and the mechanotransducing networks that organize to effectively facilitate formation of the trabeculated four-chambered heart.

Publisher

American Physiological Society

Subject

Physiology (medical),Cardiology and Cardiovascular Medicine,Physiology

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