Dataset Information

Spontaneous termination of chaotic spiral wave dynamics in human cardiac ion channel models.

ABSTRACT: Chaotic spiral or scroll wave dynamics can be found in diverse systems. In cardiac dynamics, spiral or scroll waves of electrical excitation determine the dynamics during life-threatening arrhythmias like ventricular fibrillation. In numerical studies it was found that chaotic episodes of spiral and scroll waves can be transient, thus they terminate spontaneously. We show in this study that this behavior can also be observed using models which describe the ion channel dynamics of human cardiomyocytes (Bueno-Orovio-Cherry-Fenton model and the Ten Tusscher-Noble-Noble-Panfilov model). For both models we find that the average lifetime of the chaotic transients grows exponentially with the system size. With this behavior, we classify the systems into the group of type-II supertransients. We observe a significant difference of the breakup behavior between the models, which results in a distinct dynamics during the final phase just before the termination. The observation of a (temporally) stable single-spiral state affects the prevailing description of the dynamics of type-II supertransients as being "quasi-stationary" and also the feasibility of predicting the spontaneous termination of the spiral wave dynamics. In the long term, the relation between the breakup behavior of spiral waves and properties of chaotic transients like predictability or average transient lifetime may contribute to an improved understanding and classification of cardiac arrhythmias.

SUBMITTER: Aron M

PROVIDER: S-EPMC6713330 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Spontaneous termination of chaotic spiral wave dynamics in human cardiac ion channel models.

Aron Marcel M Herzog Sebastian S Parlitz Ulrich U Luther Stefan S Lilienkamp Thomas T

PloS one 20190828 8

Chaotic spiral or scroll wave dynamics can be found in diverse systems. In cardiac dynamics, spiral or scroll waves of electrical excitation determine the dynamics during life-threatening arrhythmias like ventricular fibrillation. In numerical studies it was found that chaotic episodes of spiral and scroll waves can be transient, thus they terminate spontaneously. We show in this study that this behavior can also be observed using models which describe the ion channel dynamics of human cardiomyo ...[more]

PMID: 31461472

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Project description:Computational modeling of cardiac electrophysiology (EP) has recently transitioned from a scientific research tool to clinical applications. To ensure reliability of clinical or regulatory decisions made using cardiac EP models, it is vital to evaluate the uncertainty in model predictions. Model predictions are uncertain because there is typically substantial uncertainty in model input parameters, due to measurement error or natural variability. While there has been much recent uncertainty quantification (UQ) research for cardiac EP models, all previous work has been limited by either: (i) considering uncertainty in only a subset of the full set of parameters; and/or (ii) assigning arbitrary variation to parameters (e.g., ±10 or 50% around mean value) rather than basing the parameter uncertainty on experimental data. In our recent work we overcame the first limitation by performing UQ and sensitivity analysis using a novel canine action potential model, allowing all parameters to be uncertain, but with arbitrary variation. Here, we address the second limitation by extending our previous work to use data-driven estimates of parameter uncertainty. Overall, we estimated uncertainty due to population variability in all parameters in five currents active during repolarization: inward potassium rectifier, transient outward potassium, L-type calcium, rapidly and slowly activating delayed potassium rectifier; 25 parameters in total (all model parameters except fast sodium current parameters). A variety of methods was used to estimate the variability in these parameters. We then propagated the uncertainties through the model to determine their impact on predictions of action potential shape, action potential duration (APD) prolongation due to drug block, and spiral wave dynamics. Parameter uncertainty had a significant effect on model predictions, especially L-type calcium current parameters. Correlation between physiological parameters was determined to play a role in physiological realism of action potentials. Surprisingly, even model outputs that were relative differences, specifically drug-induced APD prolongation, were heavily impacted by the underlying uncertainty. This is the first data-driven end-to-end UQ analysis in cardiac EP accounting for uncertainty in the vast majority of parameters, including first in tissue, and demonstrates how future UQ could be used to ensure model-based decisions are robust to all underlying parameter uncertainties.

Project description:Regular electrical activation waves in cardiac tissue lead to the rhythmic contraction and expansion of the heart that ensures blood supply to the whole body. Irregularities in the propagation of these activation waves can result in cardiac arrhythmias, like ventricular tachycardia (VT) and ventricular fibrillation (VF), which are major causes of death in the industrialised world. Indeed there is growing consensus that spiral or scroll waves of electrical activation in cardiac tissue are associated with VT, whereas, when these waves break to yield spiral- or scroll-wave turbulence, VT develops into life-threatening VF: in the absence of medical intervention, this makes the heart incapable of pumping blood and a patient dies in roughly two-and-a-half minutes after the initiation of VF. Thus studies of spiral- and scroll-wave dynamics in cardiac tissue pose important challenges for in vivo and in vitro experimental studies and for in silico numerical studies of mathematical models for cardiac tissue. A major goal here is to develop low-amplitude defibrillation schemes for the elimination of VT and VF, especially in the presence of inhomogeneities that occur commonly in cardiac tissue. We present a detailed and systematic study of spiral- and scroll-wave turbulence and spatiotemporal chaos in four mathematical models for cardiac tissue, namely, the Panfilov, Luo-Rudy phase 1 (LRI), reduced Priebe-Beuckelmann (RPB) models, and the model of ten Tusscher, Noble, Noble, and Panfilov (TNNP). In particular, we use extensive numerical simulations to elucidate the interaction of spiral and scroll waves in these models with conduction and ionic inhomogeneities; we also examine the suppression of spiral- and scroll-wave turbulence by low-amplitude control pulses. Our central qualitative result is that, in all these models, the dynamics of such spiral waves depends very sensitively on such inhomogeneities. We also study two types of control schemes that have been suggested for the control of spiral turbulence, via low amplitude current pulses, in such mathematical models for cardiac tissue; our investigations here are designed to examine the efficacy of such control schemes in the presence of inhomogeneities. We find that a local pulsing scheme does not suppress spiral turbulence in the presence of inhomogeneities; but a scheme that uses control pulses on a spatially extended mesh is more successful in the elimination of spiral turbulence. We discuss the theoretical and experimental implications of our study that have a direct bearing on defibrillation, the control of life-threatening cardiac arrhythmias such as ventricular fibrillation.

Dataset Information

Spontaneous termination of chaotic spiral wave dynamics in human cardiac ion channel models.

Publications

Spontaneous termination of chaotic spiral wave dynamics in human cardiac ion channel models.

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