Electromechanical vortex filaments during cardiac fibrillation

J. Christoph, M. Chebbok, C. Richter, J. Schröder-Schetelig, P. Bittihn, S. Stein, I. Uzelac, F. H. Fenton, G. Hasenfuß, R. F. Gilmour Jr., S. Luther

Self-organized dynamics of vortex-like rotating waves or scroll waves underlie complex spatial-temporal pattern formation in many excitable chemical and biological systems1-4. In the heart, filament-like phase singularities5,6associated with three-dimensional scroll waves8are considered to be the organizing centers of life-threatening cardiac arrhythmias7-13. The mechanisms underlying the onset, perpetuation, and control14-16of electromechanical turbulence in the heart are inherently three-dimensional phenomena. However, the visualization of three-dimensional spatial-temporal dynamics of scroll waves inside cardiac tissue has thus far evaded experimental realization. Here, we show that three-dimensional mechanical scroll waves and filament-like phase singularities can be observed deep inside contracting cardiac tissue using high-resolution 4D ultrasound-based strain imaging. We found that mechanical phase singularities co-exist with electrical phase singularities during cardiac fibrillation. We investigated the dynamics of electrical and mechanical phase singularities using simultaneous tri-modal measurement of membrane potential, intracellular calcium, and mechanical contraction of the heart. Our results demonstrate that cardiac fibrillation can be characterized through the three-dimensional spatial-temporal dynamics of mechanical phase singularities, which arise inside the fibrillating contracting ventricular wall. We demonstrate that electrical and mechanical phase singularities show complex interaction and we characterize their dynamics in terms of trajectories, topological charge, and lifetime. We anticipate that our findings will provide novel perspectives for non-invasive diagnostic imaging and therapeutic applications.