Cardiac Re-entry Dynamics and Self-termination in DT-MRI Based Model of Human Fetal Heart

Irina V Biktasheva,Fen Cai Wen,Arun V Holden,Richard A Anderson,Eleftheria Pervolaraki

doi:10.3389/fphy.2018.00015

Abstract

The effect of human foetal heart geometry and anisotropy on anatomy induced drift and self-termination of cardiac re-entry is studied here in MRI based 2D slice and 3D whole heart computer simulations. Isotropic and anisotropic models of 20 weeks of gestational age human foetal heart obtained from 100μm voxel diffusion tensor MRI data sets were used in the computer simulations. The fiber orientation angles of the heart were obtained from the orientation of the DT-MRI primary eigenvectors. In a spatially homogeneous electrophysiological monodomain model with the DT-MRI based heart geometries, cardiac re-entry was initiated at a prescribed location in a 2D slice, and in the 3D whole heart anatomy models. Excitation was described by simplified FitzHugh-Nagumo kinetics. In a slice of the heart, with propagation velocity twice as fast along the fibres than across the fibers, DT-MRI based fiber anisotropy changes the re-entry dynamics from pinned to an anatomical re-entry. In the 3D whole heart models, the fiber anisotropy changes cardiac re-entry dynamics from a persistent re-entry to the re-entry self-termination. The self-termination time depends on the re-entry’s initial position. In all the simulations with the DT-MRI based cardiac geometry, the anisotropy of the myocardial tissue shortens the time to re-entry self-termination several folds. The numerical simulations depend on the validity of the DT-MRI data set used. The ventricular wall showed the characteristic transmural rotation of the helix angle of the developed mammalian heart, while the fiber orientation in the atria was irregular.

Highlights

The re-entry does not terminate at the inexcitable boundaries, but after a faster than in the previous isotropic case transient, compare the time units labels in the Figures 2A,B, the anisotropy of the medium turns the initial spiral wave into the fast anatomical re-entry around the septum cuneiform opening, see Figure 2B
The role of heart anatomy and anisotropy in the origin and sustainability of cardiac arrhythmias has been appreciated for a long time, there is limited experimental evidence to clarify detail of the heart anatomy effect on persistent cardiac arrhythmias and fibrillation
The combination of the High Performance Computing with the high-resolution DT-MRI based anatomy models of the heart allows anatomically realistic in silico testing of the effects of individual heart anatomy and anisotropy on the cardiac re-entry dynamics [34, 43, 44, 49, 56]

Summary

Introduction

Since the over a century ago hypothesis that cardiac re-entry underlies cardiac arrhythmias [1, 2], and the much later confirmation of the hypothesis in cardiac tissue experiment [3, 4], the reentry (aka spiral wave in 2D, cardiac excitation vortex in 3D), its origin and its role in sustained arrhythmias and fibrillation, as well as a possibility of its effective control and defibrillation, have been an object of extensive theoretical study and modeling [5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20]. That the anisotropic discontinuities observed in healthy hearts, and shown to be consistent within a species, might have been suspected to facilitate initiation of arrhythmias

Methods

Results

Conclusion