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Effects of early afterdepolarizations on excitation patterns in an accurate model of the human ventricles

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  • Enid Van Nieuwenhuyse
  • Gunnar Seemann
  • Alexander V Panfilov
  • Nele Vandersickel

Abstract

Early Afterdepolarizations, EADs, are defined as the reversal of the action potential before completion of the repolarization phase, which can result in ectopic beats. However, the series of mechanisms of EADs leading to these ectopic beats and related cardiac arrhythmias are not well understood. Therefore, we aimed to investigate the influence of this single cell behavior on the whole heart level. For this study we used a modified version of the Ten Tusscher-Panfilov model of human ventricular cells (TP06) which we implemented in a 3D ventricle model including realistic fiber orientations. To increase the likelihood of EAD formation at the single cell level, we reduced the repolarization reserve (RR) by reducing the rapid delayed rectifier Potassium current and raising the L-type Calcium current. Varying these parameters defined a 2D parametric space where different excitation patterns could be classified. Depending on the initial conditions, by either exciting the ventricles with a spiral formation or burst pacing protocol, we found multiple different spatio-temporal excitation patterns. The spiral formation protocol resulted in the categorization of a stable spiral (S), a meandering spiral (MS), a spiral break-up regime (SB), spiral fibrillation type B (B), spiral fibrillation type A (A) and an oscillatory excitation type (O). The last three patterns are a 3D generalization of previously found patterns in 2D. First, the spiral fibrillation type B showed waves determined by a chaotic bi-excitable regime, i.e. mediated by both Sodium and Calcium waves at the same time and in same tissue settings. In the parameter region governed by the B pattern, single cells were able to repolarize completely and different (spiral) waves chaotically burst into each other without finishing a 360 degree rotation. Second, spiral fibrillation type A patterns consisted of multiple small rotating spirals. Single cells failed to repolarize to the resting membrane potential hence prohibiting the Sodium channel gates to recover. Accordingly, we found that Calcium waves mediated these patterns. Third, a further reduction of the RR resulted in a more exotic parameter regime whereby the individual cells behaved independently as oscillators. The patterns arose due to a phase-shift of different oscillators as disconnection of the cells resulted in continuation of the patterns. For all patterns, we computed realistic 9 lead ECGs by including a torso model. The B and A type pattern exposed the behavior of Ventricular Tachycardia (VT). We conclude that EADs at the single cell level can result in different types of cardiac fibrillation at the tissue and 3D ventricle level.

Suggested Citation

  • Enid Van Nieuwenhuyse & Gunnar Seemann & Alexander V Panfilov & Nele Vandersickel, 2017. "Effects of early afterdepolarizations on excitation patterns in an accurate model of the human ventricles," PLOS ONE, Public Library of Science, vol. 12(12), pages 1-19, December.
  • Handle: RePEc:plo:pone00:0188867
    DOI: 10.1371/journal.pone.0188867
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    References listed on IDEAS

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    1. David F. Richards & James N. Glosli & Erik W. Draeger & Arthur A. Mirin & Bor Chan & Jean-luc Fattebert & William D. Krauss & Tomas Oppelstrup & Chris J. Butler & John A. Gunnels & Viatcheslav Gurev &, 2013. "Towards real-time simulation of cardiac electrophysiology in a human heart at high resolution," Computer Methods in Biomechanics and Biomedical Engineering, Taylor & Francis Journals, vol. 16(7), pages 802-805, July.
    2. Soling Zimik & Nele Vandersickel & Alok Ranjan Nayak & Alexander V Panfilov & Rahul Pandit, 2015. "A Comparative Study of Early Afterdepolarization-Mediated Fibrillation in Two Mathematical Models for Human Ventricular Cells," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-20, June.
    3. Nele Vandersickel & Ivan V Kazbanov & Anita Nuitermans & Louis D Weise & Rahul Pandit & Alexander V Panfilov, 2014. "A Study of Early Afterdepolarizations in a Model for Human Ventricular Tissue," PLOS ONE, Public Library of Science, vol. 9(1), pages 1-19, January.
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    Cited by:

    1. Roman Rokeakh & Tatiana Nesterova & Konstantin Ushenin & Ekaterina Polyakova & Dmitry Sonin & Michael Galagudza & Tim De Coster & Alexander Panfilov & Olga Solovyova, 2021. "Anatomical Model of Rat Ventricles to Study Cardiac Arrhythmias under Infarction Injury," Mathematics, MDPI, vol. 9(20), pages 1-27, October.
    2. André H. Erhardt, 2018. "Bifurcation Analysis of a Certain Hodgkin-Huxley Model Depending on Multiple Bifurcation Parameters," Mathematics, MDPI, vol. 6(6), pages 1-15, June.

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