The importance of Purkinje activation in long duration ventricular fibrillation

Abstract

Background: The mechanisms that maintain long duration ventricular fibrillation (LDVF) are unclear. The difference in distribution of the Purkinje system in dogs and pigs was explored to determine if Purkinje activation propagates to stimulate working myocardium (WM) during LDVF and WM pacing.

Methods and results: In-vivo extracellular recordings were made from 1044 intramural plunge and epicardial plaque electrodes in 6 pig and 6 dog hearts. Sinus activation propagated sequentially from the endocardium to the epicardium in dogs but not pigs. During epicardial pacing, activation propagated along the endocardium and traversed the LV wall almost parallel to the epicardium in dogs, but in pigs propagated away from the pacing site approximately perpendicular to the epicardium. After 1 minute of VF, activation rate near the endocardium was significantly faster than near the epicardium in dogs (P<0.01) but not pigs (P>0.05). From 2 to 10 minutes of LDVF, recordings exhibiting Purkinje activations were near the endocardium in dogs (P<0.01) but were scattered transmurally in pigs, and the WM activation rate in recordings in which Purkinje activations were present was significantly faster than the WM activation rate in recordings in which Purkinje activations were absent (P<0.01). In 10 isolated perfused dog hearts, the LV endocardium was exposed and 2 microelectrodes were inserted into Purkinje and adjacent myocardial cells. After 5 minutes of LDVF, mean Purkinje activation rate was significantly faster than mean WM activation rate (P<0.01).

Conclusion: These extracellular and intracellular findings about activation support the hypothesis that Purkinje activation propagates to stimulate WM during sinus rhythm, pacing, and LDVF.

Keywords: arrhythmia (mechanisms); long duration ventricular fibrillation; ventricular arrhythmia.

Figure 1.

Diagram of the (A) plaque electrodes, (B) plunge needle electrodes, (C) geometry of the plaque and needle electrodes, and (D) location of the electrodes on the heart. Asterisks indicate sites of pacing electrodes.

Figure 2.

Voltage electrograms (top) and their first temporal derivative (bottom) from the 4 most distal electrodes from a plunge needle during sinus rhythm. The most distal electrode (1) was in the ventricular cavity.

Figure 3.

Epicardial activation during sinus rhythm in a pig. Each red colored pixel is an electrode site at which the rate of voltage change (dV/dt) is ≤−0.5 V/s sometime during the 1‐ms interval represented by each frame. The numbers show the time immediately before a sinus activation propagates into the mapped region.

Figure 4.

Epicardial activation during pacing from an epicardial site below the bottom edge of the mapping plaque in a pig. Each red colored pixel is an electrode site at which the rate of voltage change (dV/dt) is ≤−0.5 V/s sometime during the 1.5‐ms interval represented by each frame. The numbers show the time 2 ms after the pacing stimulus.

Figure 5.

The 12 unipolar recordings from 1 plunge needle during sinus rhythm in a dog (A) and a pig (B). The activation complex within the box on the left is shown at a greater time scale on the right. The times of fastest downslope are indicated on the right with endocardial activation labeled 0 ms.

Figure 6.

Activation during pacing from the epicardial site marked as * at the edge of a transmural plane of plunge electrodes in (A) a dog and (B) a pig. Each colored pixel (red for dog and yellow for pig) is an electrode site at which the rate of voltage change (dV/dt) is ≤−0.5 V/s sometime during the 3‐ms interval represented by each frame. The numbers show the time from the beginning of the pacing stimulus. Endo indicates endocardial most layer; Epi, epicardial most layer of electrodes. See text for detailed explanation.

Figure 7.

Transmural activation rate maps 1, 4, and 8 minutes after VF induction in a dog (left) and a pig (right). The top map is for the horizontal row of plunge needles and the bottom map is for the vertical row. The epicardium is at the top of each map and the endocardium is at the bottom. The color bar indicates the activation rate in Hz. After 1 minute of VF, the activation rate was similar transmurally in both species. After 4 minutes of long duration ventricular fibrillation (LDVF), fastest activation was in the endocardial layer and gradually decreased from endo‐ to epicardium in the dog, but was distributed among epicardial, mid‐, and endocardial layers in the pig. After 8 minutes of LDVF in the dog, the endocardial layer still activated while the epicardial layer was almost silent. In the pig, the fastest activation area was still scattered among the 3 layers.

Figure 8.

Dog and pig single plunge needle recordings during VF (top traces). Bottom 2 traces are electrograms and the first temporal derivative of the electrograms expanded from the 3 activation complexes in squares in the top traces. Endo indicates endocardial most electrode; Epi, epicardial most electrode; P, Purkinje activation; VF, ventricular fibrillation; WM, working myocardial activation.

Figure 9.

Mean and SD of WM activation rates in recordings with and without Purkinje activations every minute during VF. A, is for the most endocardial electrodes of each plunge needle in dogs. B, for all plunge needle electrodes within the ventricular wall in pigs. Percent changes of activation rate at each minute between recordings with and without Purkinje activations during VF are superimposed on the bar graphs. An asterisk indicates P<0.05 for that minute of VF. VF indicates ventricular fibrillation; WM, working myocardium.

Figure 10.

Per minute percent decreases of activation rate between recordings with and without Purkinje activation during 10 minutes of ventricular fibrillation (VF). A, for the most endocardial electrode of each plunge needle in dogs. B, for all plunge needle electrodes within the ventricular wall in pigs.

Figure 11.

Two simultaneous microelectrode recordings every minute for 10 minutes during LDVF in a dog. The top tracing is from a microelectrode inserted into a WM. The bottom tracing is from a microelectrode inserted into a Purkinje fiber (P) at the insertion of a false tendon about 1 mm away. Between 2 and 4 minutes of LDVF, the Purkinje activation leads the WM activation in a one‐to‐one relationship. After 4 minutes of LDVF, Purkinje activations are more rapid than WM activations. LDVF indicates long duration ventricular fibrillation; WM, working myocardium.

Figure 12.

Mean and SDs of activation rates of Purkinje and WM cells during 10 minutes of LDVF. Percent changes of activation rate between Purkinje and WM are superimposed on the bar graphs. *P<0.01 vs the activation rate of Purkinje cells. LDVF indicates long duration ventricular fibrillation; WM, working myocardium.

Figure 13.

Per minute percent decrease of activation rate between recordings of Purkinje (green) and WM (red) during 10 minutes of VF. VF indicates ventricular fibrillation; WM, working myocardium.