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Effects of electroporation on optically recorded transmembrane potential responses to high-intensity electrical shocks

¹Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio 44106; and ²Institut Non Linéaire de Nice, Centre National de la Recherche Scientifique, 06560 Valbonne, France

Submitted 24 July 2003 ; accepted in final form 25 September 2003

The outcome of defibrillation shocks is determined by the nonlinear transmembrane potential (V_m) response induced by a strong external electrical field in cardiac cells. We investigated the contribution of electroporation to V_m transients during high-intensity shocks using optical mapping. Rectangular and ramp stimuli (10–20 ms) of different polarities and intensities were applied to the rabbit heart epicardium during the plateau phase of the action potential (AP). V_m were optically recorded under a custom 6-mm-diameter electrode using a voltage-sensitive dye. A gradual increase of cathodal and well as anodal stimulus strength was associated with 1) saturation and subsequent reduction of V_m; 2) postshock diastolic resting potential (RP) elevation; and 3) postshock AP amplitude (APA) reduction. Weak stimuli induced a monotonic V_m response and did not affect the RP level. Strong shocks produced a nonmonotonic V_m response and caused RP elevation and a reduction of postshock APA. The maximum positive and maximum negative V_m were recorded at 170 ± 20 mA/cm² for cathodal stimuli and at 240 ± 30 mA/cm² for anodal stimuli, respectively (means ± SE, n = 8, P = 0.003). RP elevation reached 10% of APA at a stimulus strength of 320 ± 40 mA/cm² for both polarities. Strong ramp stimuli (20 ms, 600 mA/cm²) induced a nonmonotonic V_m response, reaching the same largest positive and negative values as for rectangular shocks. The transition from monotonic to nonmonotonic morphology correlates with RP elevation and APA reduction, which is consistent with cell membrane electroporation. Strong shocks resulted in propidium iodide uptake, suggesting sarcolemma electroporation. In conclusion, electroporation is a likely explanation of the saturation and nonmonotonic nature of cellular responses reported for strong electric stimuli.

defibrillation; arrhythmia; electrophysiology; cardiac tissue electrical damage

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