Spatiotemporal Organization of Electromechanical Phase Singularities during High-Frequency Cardiac Arrhythmias

Abstract

Ventricular fibrillation (VF) is a life-threatening electromechanical dysfunction of the heart associated with complex spatiotemporal dynamics of electrical excitation and mechanical contraction of the heart muscle. It has been hypothesized that VF is driven by three-dimensional rotating electrical scroll waves, which can be characterized by filamentlike electrical phase singularities or vortex filaments, but visualizing their dynamics has been a long-standing challenge. Recently, it was shown that rotating excitation waves during VF are associated with rotating waves of mechanical deformation. Three-dimensional mechanical scroll waves and mechanical filaments describing their rotational core regions were observed in the ventricles by using high-resolution ultrasound. The findings suggest that the spatiotemporal organization of cardiac fibrillation may be assessed from waves of mechanical deformation. However, the complex relationship between excitation and mechanical waves during VF is currently not understood. Here, we study the fundamental nature of mechanical phase singularities, their spatiotemporal organization, and their relation with electrical phase singularities. We demonstrate the existence of two fundamental types of mechanical phase singularities: “paired singularities,” which are colocalized with electrical phase singularities, and “unpaired singularities,” which can form independently. We show that the unpaired singularities emerge due to the anisotropy of the active force field, generated by fiber anisotropy in cardiac tissue, and the nonlocality of elastic interactions, which jointly induce strong spatiotemporal inhomogeneities in the strain fields. The inhomogeneities lead to the breakup of deformation waves and create mechanical phase singularities, even in the absence of electrical singularities, which are typically associated with excitation wave break. We exploit these insights to develop an approach to discriminate paired and unpaired mechanical phase singularities, which could potentially be used to locate electrical rotor cores from a mechanical measurement. Our findings provide a fundamental understanding of the complex spatiotemporal organization of electromechanical waves in the heart and a theoretical basis for the analysis of high-resolution ultrasound data for the three-dimensional mapping of heart rhythm disorders.