Low-energy control of electrical turbulence in the heart

Abstract

Controlling the complex spatio-temporal dynamics underlying life-threatening cardiac arrhythmias such as fibrillation is extremely difficult due to the nonlinear interaction of excitation waves within a heterogeneous anatomical substrate1–4. Lacking a better strategy, strong, globally resetting electrical shocks remain the only reliable treatment for cardiac fibrillation5–7. Here, we establish the relation between the response of the tissue to an electric field and the spatial distribution of heterogeneities of the scale-free coronary vascular structure. We show that in response to a pulsed electric field E, these heterogeneities serve as nucleation sites for the generation of intramural electrical waves with a source density ρ(E), and a characteristic time τ for tissue depolarization that obeys a power law τ∝Eα. These intramural wave sources permit targeting of electrical turbulence near the cores of the vortices of electrical activity that drive complex fibrillatory dynamics. We show in vitro that simultaneous and direct access to multiple vortex cores results in rapid synchronization of cardiac tissue and therefore efficient termination of fibrillation. Using this novel control strategy, we demonstrate, for the first time, low-energy termination of fibrillation in vivo. Our results give new insights into the mechanisms and dynamics underlying the control of spatio-temporal chaos in heterogeneous excitable media and at the same time provide new research perspectives towards alternative, life-saving low-energy defibrillation techniques.

Control of electrical turbulence by periodic excitation of cardiac tissue

“…The mechanism how multiple low-energy far-field pulses terminate arrhythmias are not well understood as experimental methods to visualize three dimensional electrical turbulence are missing. Luther et al 13 suggest that the major conduction heterogeneities necessary for LEAP are given by large coronary arteries and show that the size distribution of the heterogeneities follows a power law. However, Caldwell et al 23 did not find such a co-localization of hot spots and major coronary vessels.…”

“…These adverse effects could be diminished if VF could be terminated reliably by defibrillation shocks with significantly lower energies. Recent studies 12,13 of AF in vitro and in vivo as well as VF in vitro have shown that a sequence of five low-energy far-field pulses with stimulation rates close to the arrhythmia cycle length can require 80 − 90% less energy per pulse than a single shock. This method is called low-energy antifibrillation pacing (LEAP).…”

“…The simplicity of our composite model allows us to perform systematic statistical studies with a set of 100 initial conditions. This is essential since both standard defibrillation and LEAP may depend critically on these and are also associated with large uncertainties 13 .…”

“…Very similar results are found in both cases and, moreover, the size distribution of the radii of arteries are found to be almost identical for atria and ventricles. Therefore, we expect that LEAP can be qualitatively investigated within a simple two dimensional model in which the non-conducting heterogeneities are represented by circles whose size distribution is given by the distribution of radii of coronary arteries measured in 13 . Furthermore, we employed three alternative models which are established for ventricular cells [32][33][34] .…”

“…For LEAP, reduction of defibrillation energy is the quantity which is studied in the quasi-two-dimensional AF and the three dimensional VF 13 . Very similar results are found in both cases and, moreover, the size distribution of the radii of arteries are found to be almost identical for atria and ventricles.…”