Activation becomes highly organized during long-duration ventricular fibrillation in canine hearts

Abstract

Little is known about the three-dimensional (3-D) intramural activation sequences during long-duration ventricular fibrillation (VF), including the role of the subendocardium and its Purkinje fibers (PFs) in long-duration VF maintenance. Our aim was to explore the mechanism of long-duration VF maintenance with 3-D electrical mapping. We recorded 10 min of electrically induced VF in the left ventricular anterior free wall of six 10-kg, open-chest dogs using a 3-D transmural unipolar electrode matrix (9 x 9 x 6, 2-mm spacing) that allowed us to map intramural activation sequences. At 2.5 + or - 1.8 min of VF, although the body surface ECG continued to exhibit a disorganized VF pattern, intramurally a more organized, synchronous activation pattern was first observed [locally synchronized VF (LSVF)]. This pattern occurred one or more times in all dogs and was present 33.4 + or - 31.4% of the time during 5-10 min of VF. As opposed to the preceding changing complex activation sequences of VF, during LSVF, wavefronts were large and highly repeatable near the endocardium, first exciting the endocardium almost simultaneously and then rapidly spreading toward the epicardium with different levels of conduction block en route. During LSVF, PF activations always preceded working myocardium activations near the endocardium. In conclusion, long-duration VF in dogs frequently becomes highly organized in the subendocardium, with activation fronts arising in this region and passing intramurally toward the epicardium, even though the surface ECG continues to exhibit a disorganized pattern. PFs appear to play an important role during this stage of VF.

Fig. 1.

Recordings from an endocardial electrode in animal 2 during long-duration ventricullar fibrillation (VF). A–E: a 3-s electrical recording (top trace) and its dV/dt (bottom trace) during sinus rhythm (A) and at 1.7 min (B), 4.6 min (C), 5 min (D), and 10 min (E) of VF. The onset of locally synchronized VF (LSVF) is shown by the open arrow in C. F: 50-ms enlargements of the electrical recording and its dV/dt from areas 1–7 in A–E. For all images, the height of the vertical bars to the left of the electrical recording is 10 mV. The height of the vertical bars to the left of dV/dt is 0.5 mV/ms, with the top at 0 mV/ms. Purkinje fiber (PF) activations are indicated by the solid arrows.

Fig. 2.

Example of LSVF wavefront block near the epicardium in animal 6. In A, the surface ECG lead II (row 1) and recordings [rows 2–6, from the endocardium (Endo) to epicardium (Epi)] from one needle at 5.9 min of VF are shown. The most endocardial electrode recording was in the cavity and is not shown. The arrow indicates the onset of LSVF. The height of the vertical scale to the left is 10 mV and applies to all needle recordings. *Activations propagating from the endocardium that blocked before reaching the epicardium. The two dashed lines are aligned with the endocardial activations in row 2 to indicate the endocardial to epicardial spread of activation. B: the same ECG and electrical recordings at 10 min of VF.

Fig. 3.

Isochronal maps in animal 1 during sinus rhythm (A) and at 1 min of VF during non-LSVF (B) and at 4.6 (C) and 4.9 min (D) of VF during LSVF. Row 1 shows the three-dimensional isochronal maps. Rows 2–7 show the same activation sequence as in row 1, with the electrodes displayed in six planes 2-mm apart, composed of the first (epicardium) to sixth (endocardium) electrodes on all needles. ^xCavity electrodes. Circles represent electrodes located in the myocardium with color indicating the activation time according to the scale at the bottom. Open circles represent electrodes not recording activation. Circles with magenta boundaries in C and D indicate the earliest activation sites.

Fig. 4.

Endocardium-epicardium activation rate difference during long-duration VF. A: means and SDs of the block at epicardium ratio of LSVF beats every 5 s during 10 min of VF for all animals. There is no data point when no LSVF was present in any animal. B: means and SDs of activation rates every 10 s for all animals. *Activation rate of the endocardial electrodes differed significantly from that of the nonendocardial electrodes during this 10-s interval.

Fig. 5.

Wavefront descriptors in animal 2 indicating sudden changes at 4.6 min of VF. A–C: multiplicity (A), maximum wavefront extent (B), and repeatability (C) averaged every 10 s. D: distributions of nonexcited gaps. Vertical dashed lines in A–D indicate the moment of the transition from non-LSVF to LSVF.

Fig. 6.

Endocardial spatial distributions of the earliest activation sites of LSVF beats during 10 min of VF and of sinus beats. A and B: distributions in the two-dimensional projection plane composed of the endocardial electrodes from animal 1 (A) and animal 6 (B). Squares represent endocardial electrodes. The color of the square indicates the earliest activation incidence during sinus rhythm and LSVF in that electrode, according to the color bar shown at the right. Empty squares represent electrodes in which no earliest activation was observed. The electrodes recording the largest and second largest number of earliest activations have red and magenta outside boundaries.

Fig. 7.

Transition from non-LSVF to LSVF. In A and B, means and SDs of minimum dV/dt and cycle lengths during 21 cycles averaged for all animals and all electrodes are shown with the first LSVF cycle labeled cycle 0 (dashed line). C: recordings from an endocardial electrode during LSVF initiation in animal 2. Rows 1, 3, and 5 show continuous 1-s recordings (V). Rows 2, 4, and 6 show the corresponding dV/dt traces. The vertical bar at the left of the V recordings corresponds to 10 mV. The vertical bar at the left of the dV/dt traces corresponds to 0.5 mV/ms with the top at 0 mV/ms. Working myocardium (WM) and PF activations are indicated. Bold italic numbers indicate PF-WM intervals (in ms); regular numbers indicate cycle lengths (in ms) between WM activations. A few WM activations did not reach the −0.5-mV/ms threshold and were manually selected.

Fig. 8.

PF and WM activation properties in animal 2. A and B: incidence (A) and minimum dV/dt (B) of PF and WM activations. C:PF-WM intervals. Dashed lines indicate the transition to LSVF at 4.6 min of VF. The horizontal line in C corresponds to a PF-WM interval of 0 ms.