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Stochastic Termination of Spiral Wave Dynamics in Cardiac Tissue

Rotating spiral waves are self-organized features in spatially extended excitable media and may play an important role in cardiac arrhythmias including atrial fibrillation (AF). In homogeneous media, spiral wave dynamics are perpetuated through spiral wave breakup, leading to the continuous birth an...

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Autores principales: Rappel, Wouter-Jan, Krummen, David E., Baykaner, Tina, Zaman, Junaid, Donsky, Alan, Swarup, Vijay, Miller, John M., Narayan, Sanjiv M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9524168/
https://www.ncbi.nlm.nih.gov/pubmed/36187938
http://dx.doi.org/10.3389/fnetp.2022.809532
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author Rappel, Wouter-Jan
Krummen, David E.
Baykaner, Tina
Zaman, Junaid
Donsky, Alan
Swarup, Vijay
Miller, John M.
Narayan, Sanjiv M.
author_facet Rappel, Wouter-Jan
Krummen, David E.
Baykaner, Tina
Zaman, Junaid
Donsky, Alan
Swarup, Vijay
Miller, John M.
Narayan, Sanjiv M.
author_sort Rappel, Wouter-Jan
collection PubMed
description Rotating spiral waves are self-organized features in spatially extended excitable media and may play an important role in cardiac arrhythmias including atrial fibrillation (AF). In homogeneous media, spiral wave dynamics are perpetuated through spiral wave breakup, leading to the continuous birth and death of spiral waves, but have a finite probability of termination. In non-homogeneous media, however, heterogeneities can act as anchoring sources that result in sustained spiral wave activity. It is thus unclear how and if AF may terminate following the removal of putative spiral wave sources in patients. Here, we address this question using computer simulations in which a stable spiral wave is trapped by an heterogeneity and is surrounded by spiral wave breakup. We show that, following ablation of spatial heterogeneity to render that region of the medium unexcitable, termination of spiral wave dynamics is stochastic and Poisson-distributed. Furthermore, we show that the dynamics can be accurately described by a master equation using birth and death rates. To validate these predictions in vivo, we mapped spiral wave activity in patients with AF and targeted the locations of spiral wave sources using radiofrequency ablation. Targeted ablation was indeed able to terminate AF, but only after a variable delay of up to several minutes. Furthermore, and consistent with numerical simulations, termination was not accompanied by gradual temporal or spatial organization. Our results suggest that spiral wave sources and tissue heterogeneities play a critical role in the maintenance of AF and that the removal of sources results in spiral wave dynamics with a finite termination time, which could have important clinical implications.
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spelling pubmed-95241682022-09-30 Stochastic Termination of Spiral Wave Dynamics in Cardiac Tissue Rappel, Wouter-Jan Krummen, David E. Baykaner, Tina Zaman, Junaid Donsky, Alan Swarup, Vijay Miller, John M. Narayan, Sanjiv M. Front Netw Physiol Network Physiology Rotating spiral waves are self-organized features in spatially extended excitable media and may play an important role in cardiac arrhythmias including atrial fibrillation (AF). In homogeneous media, spiral wave dynamics are perpetuated through spiral wave breakup, leading to the continuous birth and death of spiral waves, but have a finite probability of termination. In non-homogeneous media, however, heterogeneities can act as anchoring sources that result in sustained spiral wave activity. It is thus unclear how and if AF may terminate following the removal of putative spiral wave sources in patients. Here, we address this question using computer simulations in which a stable spiral wave is trapped by an heterogeneity and is surrounded by spiral wave breakup. We show that, following ablation of spatial heterogeneity to render that region of the medium unexcitable, termination of spiral wave dynamics is stochastic and Poisson-distributed. Furthermore, we show that the dynamics can be accurately described by a master equation using birth and death rates. To validate these predictions in vivo, we mapped spiral wave activity in patients with AF and targeted the locations of spiral wave sources using radiofrequency ablation. Targeted ablation was indeed able to terminate AF, but only after a variable delay of up to several minutes. Furthermore, and consistent with numerical simulations, termination was not accompanied by gradual temporal or spatial organization. Our results suggest that spiral wave sources and tissue heterogeneities play a critical role in the maintenance of AF and that the removal of sources results in spiral wave dynamics with a finite termination time, which could have important clinical implications. Frontiers Media S.A. 2022-01-26 /pmc/articles/PMC9524168/ /pubmed/36187938 http://dx.doi.org/10.3389/fnetp.2022.809532 Text en Copyright © 2022 Rappel, Krummen, Baykaner, Zaman, Donsky, Swarup, Miller and Narayan. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Network Physiology
Rappel, Wouter-Jan
Krummen, David E.
Baykaner, Tina
Zaman, Junaid
Donsky, Alan
Swarup, Vijay
Miller, John M.
Narayan, Sanjiv M.
Stochastic Termination of Spiral Wave Dynamics in Cardiac Tissue
title Stochastic Termination of Spiral Wave Dynamics in Cardiac Tissue
title_full Stochastic Termination of Spiral Wave Dynamics in Cardiac Tissue
title_fullStr Stochastic Termination of Spiral Wave Dynamics in Cardiac Tissue
title_full_unstemmed Stochastic Termination of Spiral Wave Dynamics in Cardiac Tissue
title_short Stochastic Termination of Spiral Wave Dynamics in Cardiac Tissue
title_sort stochastic termination of spiral wave dynamics in cardiac tissue
topic Network Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9524168/
https://www.ncbi.nlm.nih.gov/pubmed/36187938
http://dx.doi.org/10.3389/fnetp.2022.809532
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