Mechanism of reentry induction by a 9-V battery in rabbit ventricles

Martin J Bishop,Kumaraswamy Nanthakumar,Gernot Plank,Edward J Vigmond,Gil Bub,Manish Kalla,Rebecca A B Burton

doi:10.1152/ajpheart.00591.2013

Abstract

Although the application of a 9-V battery to the epicardial surface is a simple method of ventricular fibrillation induction, the fundamental mechanisms underlying this process remain unstudied. We used a combined experimental and modelling approach to understand how the interaction of direct current (DC) from a battery may induce reentrant activity within rabbit ventricles and its dependence on battery application timing and duration. A rabbit ventricular computational model was used to simulate 9-V battery stimulation for different durations at varying onset times during sinus rhythm. Corresponding high-resolution optical mapping measurements were conducted on rabbit hearts with DC stimuli applied via a relay system. DC application to diastolic tissue induced anodal and cathodal make excitations in both simulations and experiments. Subsequently, similar static epicardial virtual electrode patterns were formed that interacted with sinus beats but did not induce reentry. Upon battery release during diastole, break excitations caused single ectopics, similar to application, before sinus rhythm resumed. Reentry induction was possible for short battery applications when break excitations were slowed and forced to take convoluted pathways upon interaction with refractory tissue from prior make excitations or sinus beats. Short-lived reentrant activity could be induced for battery release shortly after a sinus beat for longer battery applications. In conclusion, the application of a 9-V battery to the epicardial surface induces reentry through a complex interaction of break excitations after battery release with prior induced make excitations or sinus beats.

Highlights

Using advanced computational modeling combined with high-resolution optical mapping measurements, we have uncovered the hitherto unknown conditions under which DC from a battery interacts with myocardial tissue to induce reentry within rabbit ventricles
In all cases of arrhythmia induction, reentry was initiated due to the interaction of break excitations with: 1. Refractory tissue due to prior make excitations, requiring relatively short battery applications applied to diastolic tissue; 2
Reentry was induced in these circumstances as the break excitation wavefronts were slowed and forced to take convoluted pathways upon interaction with the heterogeneous distributions of refractory tissue

Summary

Computational Methods

Electrical activity was simulated by the bidomain equations within a finite-element model of the rabbit ventricle [7] using the Cardiac Arrhythmia Research Package (CARP) [26]. Ionic membrane dynamics within the myocardium were represented by a recent rabbit ventricular cell http://www.ajpheart.org. After a variable time (50 –300 ms) after the 10th paced beat, the battery electrodes were activated for a variable duration (50 –700 ms), after which activity was allowed to evolve and vulnerability for reentry induction assessed. Simulation of battery application required a bidmoain solve with a very fine time step (2 ␮s) to resolve the rapid changes in potential associated with the strong extracellular field. The heart was paced for 40 beats before the application of the battery. Activation times were found by first performing a running correlation operation on each trace with a 150-ms segment centered on an action potential upstroke captured from the middle of the imaging field and finding the local maxima of the correlation operation.

RESULTS

DISCUSSION

Summary of Arrhythmogenic Mechanisms

Study Limitations

Conclusions

DISCLOSURES