Ectopic and reentrant activation patterns in the posterior left atrium during stretch-related atrial fibrillation

Abstract

Atrial fibrillation (AF) is the most common sustained cardiac arrhythmia in humans and is predicted to dramatically increase its prevalence in the future. There is experimental evidence that increasing stretch increases the dominance of the pulmonary veins (PVs) during AF in isolated hearts and ectopic activity in the isolated PVs, but the ionic mechanisms underlying such effects are not clear and the ability of the PVs to favorably host functional reentry during stretch cannot be excluded. We used a combination of endocardial-epicardial optical mapping with phase and spectral analysis to study stretch-related AF (SRAF) in normal isolated sheep hearts. We have found rapid AF sources in the posterior left atrium (PLA) and PV region and their activation frequency and level of organization correlated with intra-atrial pressure. Analysis of the surfaces' optical mapping data in the phase domain reveals that activation of the PLA consisted of alternating patterns of breakthroughs, reentries and relatively simple waves swiping across the mapped field. The patterns on the endocardial and epicardial PLA surface at any given moment of time of the SRAF could be either identical or not identical, and the activity in the thickness of the PLA wall is hypothesized to conform to either ectopic discharge or scroll waves, but a definite evidence for the presence of such mechanisms is currently lacking. Thus the understanding of the manner by which the mechano-electric feedback effects in the PLA, including the PVs, become important in the initiation and maintenance of AF requires further detailed investigation.

Fig. 1

Schematic diagram of the experimental optical mapping setting. Up to 3-CCDs were used for simultaneous mapping of the electrical excitation patterns on the epicardium and endocardium of the atria. The endoscope used was of the flexible or the rigid (not shown) type. The panels on the right are endocardial views of the anatomy of the posterior LA wall (PLA, top) and the LA appendage and free wall (LAA, bottom). (Reproduced from Yamazaki et al., 2012).

Fig. 2

Patterns of activation in the atria-PV junction during SRAF. A) Four spatio-temporally organized periodic waves (At 0, 182, 352 and 512 ms, respectively) coming from the PLA region toward the LAA. Isochrones are plotted at 10 ms intervals. Bottom, key for the different phases of the action potential is color-coded (Reproduced from Filgueiras-Rama et al. 2011). B) Schematic directionality of activity from the PVs to LAFW (blue arrow) and from the LAFW to LSPV (red arrow) assessed at the junctional PV (JPV) region (shaded area). C) Number of activations (mean ± SEM) moving from left superior PV (LSPV) to LA free wall (LAFW) and from LAFW to LSPV (*P < 0.01 compared with LAFW to LSPV). Colors are the same as in B. (Reproduced from Kalifa et al., 2003).

Fig. 3

Complex AF dynamics at the PLA of normal sheep hearts. Sequential phase maps obtained simultaneously from PLA-endo (top row) and PLA-epi (bottom row) during AF in a sample heart. Panels a–f show synchronized patterns of excitation on the two surfaces altering from breakthroughs (a) to reentry (b), to collision (c), breakthroughs (d), coasting (e) and multiple wavebreaks and reentry (f). LSPV; left superior PV, LIPV; left inferior pulmonary vein, RPV; right PV.

Fig. 4

Examples of simultaneous and identical activation pattern on the endocardium and epicardium of the PLA of a sheep heart during SRAF. A) A representative phase snapshots from endocardial and epicardial surfaces showing synchronous rotational activity with pivoting point near the RPV. B) Synchronous breakthrough activity on the two opposing surfaces.

Fig. 5

Examples of endocardial–epicardial reentrant-breakthrough dissociated activation patterns suggesting either an L-shaped filament (A) or a U-shaped filament (B) of scroll waves.

Fig. 6

Spatial distribution of breakthrough activity in the PLA during SRAF in 4 sample isolated sheep hearts. The number of breakthroughs varies mostly in the left PVs (between 6 to 46 breakthroughs per 5 sec activity) but there is no preferential breakthrough site within the PLA. PLA; posterior LA.