Electromechanical vortex filaments during cardiac fibrillation

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Abstract

<p>The self-organized dynamics of vortex-like rotating waves, which are also known as scroll waves, are the basis of the formation of complex spatiotemporal patterns in many excitable chemical and biological systems. In the heart, filament-like phase singularities<a href="https://www.nature.com/articles/nature26001#ref5&quot; id="ref-link-abstract-5" title=" filament instability and fibrillation. Chaos 8, 20–47 (1998)">5</a>,<a href="https://www.nature.com/articles/nature26001#ref6&quot; id="ref-link-abstract-6" title=" simplifying complexity in computational models of ventricular fibrillation. Prog. Biophys. Mol. Biol. 90, 378–398 (2006)">6</a>&nbsp;that are associated with three-dimensional scroll waves<a href="https://www.nature.com/articles/nature26001#ref7&quot; id="ref-link-abstract-7" title="Winfree, A. T. Electrical turbulence in three-dimensional heart muscle. Science 266, 1003–1006 (1994)">7</a>&nbsp;are considered to be the organizing centres of life-threatening cardiac arrhythmias. The mechanisms that underlie the onset, maintenance and control<a href="https://www.nature.com/articles/nature26001#ref14&quot; id="ref-link-abstract-15" title="Fenton, F. H. et al. Termination of atrial fibrillation using pulsed low-energy far-field stimulation. Circulation 120, 467–476 (2009)">14</a>,<a href="https://www.nature.com/articles/nature26001#ref15&quot; id="ref-link-abstract-16" title="Luther, S. et al. Low-energy control of electrical turbulence in the heart. Nature 475, 235–239 (2011)">15</a>,<a href="https://www.nature.com/articles/nature26001#ref16&quot; id="ref-link-abstract-17" title="Janardhan, A. H. et al. A novel low-energy electrotherapy that terminates ventricular tachycardia with lower energy than a biphasic shock when antitachycardia pacing fails. J. Am. Coll. Cardiol. 60, 2393–2398 (2012)">16</a>&nbsp;of electromechanical turbulence in the heart are inherently three-dimensional phenomena. However, it has not previously been possible to visualize the three-dimensional spatiotemporal dynamics of scroll waves inside cardiac tissues. Here we show that three-dimensional mechanical scroll waves and filament-like phase singularities can be observed deep inside the contracting heart wall using high-resolution four-dimensional 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 by simultaneously measuring the membrane potential, intracellular calcium concentration and mechanical contractions of the heart. We show that cardiac fibrillation can be characterized using the three-dimensional spatiotemporal dynamics of mechanical phase singularities, which arise inside the fibrillating contracting ventricular wall. We demonstrate that electrical and mechanical phase singularities show complex interactions 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.</p>

Year of Publication

2018
Journal

Nature
Volume

555
Number of Pages

667+
DOI

https://doi.org/10.1038/nature26001
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