Detrimental effects of electrical fields on cardiac muscle

The use of controlled electrical shock as a therapy to manage cardiac arrhythmia is a practice commonly used today. High intensity electrical fields are generated near the shock electrodes, and if the electrodes are placed directly on or inside the heart as is often the case, tissue injury and dysfunction may result if the shock intensity is too high. Many factors influence the degree of dysfunction, including the intensity of the shock poise, duration of the pulse, waveform shape, size and position of the electrodes, and physiological state of the heart. One of the most immediate indications of aberrant cardiac function is an abnormality in the electrocardiogram, which results from field-induced changes in cellular electrophysiology. This article reviews results obtained primarily from animal experiments which delineate the intensities of electrical field that produce electrical dysfunction at various structural levels of the heart. Possible mechanisms underlying the detrimental effects of electrical fields are presented with the main focus on electroporation of the cell membrane. Other mechanisms that are described include formation of oxygen-derived free radicals, conformational damage to ionic pumps/channels, barotrauma, and hyperthermia. Differences between cathodal and anodal shock effects, as well as factors which may ameliorate electrical field-induced cardiac dysfunction, are also discussed.

[1]  Leslie Tung,et al.  Effects of Strong Electrical Shock on Cardiac Muscle Tissue a , 1994, Annals of the New York Academy of Sciences.

[2]  T. Guarnieri,et al.  Increased Pacing Threshold After an Automatic Defibrillator Shock in Dogs: Effects of Class I and Class II Antiarrhythmic Drugs , 1988, Pacing and clinical electrophysiology : PACE.

[3]  R. Hauer,et al.  Ventricular Tachycardia After In Vivo DC Shock Ablation in Dogs: Electrophysiologic and Histologic Correlation , 1991, Circulation.

[4]  L Tung,et al.  Cell-attached patch clamp study of the electropermeabilization of amphibian cardiac cells. , 1991, Biophysical journal.

[5]  L. Mcdonald,et al.  Complications in 220 patients with cardiac dysrhythmias treated by phased direct current shock, and indications for electroconversion. , 1967, British heart journal.

[6]  Patton Jn,et al.  The effects of shock energy, propranolol, and verapamil on cardiac damage caused by transthoracic countershock. , 1984 .

[7]  James C. Weaver,et al.  Electroporation: a unified, quantitative theory of reversible electrical breakdown and mechanical rupture in artificial planar bilayer membranes☆ , 1991 .

[8]  L. Opie,et al.  Effects of oxygen free radicals on isolated cardiac myocytes from guinea-pig ventricle: electrophysiological studies. , 1992, Journal of molecular and cellular cardiology.

[9]  Robert Plonsey,et al.  Stimulation of Spheroidal Cells - The Role of Cell Shape , 1976, IEEE Transactions on Biomedical Engineering.

[10]  P. Troup,et al.  Implantable cardioverters and defibrillators. , 1989, Current problems in cardiology.

[11]  J. Jones,et al.  Dysfunction and safety factor strength-duration curves for biphasic defibrillator waveforms. , 1994, The American journal of physiology.

[12]  P. S. Chen,et al.  Effect of capacitor size and pathway resistance on defibrillation threshold for implantable defibrillators. , 1994, Circulation.

[13]  M W Kroll,et al.  Smaller Capacitors Improve the Biphasic Waveform , 1994, Journal of cardiovascular electrophysiology.

[14]  J. Jones,et al.  Determination of safety factor for defibrillator waveforms in cultured heart cells. , 1982, The American journal of physiology.

[15]  E. Tekle,et al.  Electro-permeabilization of cell membranes: effect of the resting membrane potential. , 1990, Biochemical and biophysical research communications.

[16]  J. Weaver,et al.  Electroporation: A general phenomenon for manipulating cells and tissues , 1993, Journal of cellular biochemistry.

[17]  L. Chernomordik,et al.  The electrical breakdown of cell and lipid membranes: the similarity of phenomenologies. , 1987, Biochimica et biophysica acta.

[18]  L A Geddes,et al.  Therapeutic indices for transchest defibrillator shocks: effective, damaging, and lethal electrical doses. , 1980, American heart journal.

[19]  M. Josephson,et al.  ELECTROCARDIOGRAPHY Electrocardiographic changes after cardioversion of ventricular arrhythmias , 2005 .

[20]  A. Adgey,et al.  Metabolic Changes and Mitochondrial Dysfunction Early Following Transthoracic Countershock in Dogs , 1989, Pacing and clinical electrophysiology : PACE.

[21]  Electrical Trauma: Electrical injury to heart muscle cells , 1992 .

[22]  W. Stevenson,et al.  Dysrhythmias after direct-current cardioversion. , 1986, The American journal of cardiology.

[23]  R E Ideker,et al.  Ventricular defibrillation using biphasic waveforms: the importance of phasic duration. , 1989, Journal of the American College of Cardiology.

[24]  H. Greene,et al.  Catheter-mediated electrical ablation: the relation between current and pulse width on voltage breakdown and shock-wave generation. , 1988, Pacing and clinical electrophysiology : PACE.

[25]  K. Stringer,et al.  Electrolysis-induced myocardial dysfunction. A novel method for the study of free radical mediated tissue injury. , 1986, Journal of pharmacological methods.

[26]  P. Wolf,et al.  The Probability of Defibrillation Success and the Incidence of Postshock Arrhythmia as a Function of Shock Strength , 1994, Pacing and clinical electrophysiology : PACE.

[27]  T. Tsong,et al.  Electroporation of cell membranes. , 1991, Biophysical journal.

[28]  I Kodama,et al.  Aftereffects of high-intensity DC stimulation on the electromechanical performance of ventricular muscle. , 1994, The American journal of physiology.

[29]  R. Lee,et al.  Altered ion channel conductance and ionic selectivity induced by large imposed membrane potential pulse. , 1994, Biophysical journal.

[30]  L. Chernomordik,et al.  The voltage-induced local defects in unmodified BLM , 1980 .

[31]  P. Wolf,et al.  Conduction disturbances caused by high current density electric fields. , 1990, Circulation research.

[32]  L. Chernomordik,et al.  Reversible large-scale deformations in the membranes of electrically-treated cells: electroinduced bleb formation. , 1990, Biochimica et biophysica acta.

[33]  M. Morad,et al.  Role of Ca2+ channel in development of tension in heart muscle. , 1987, Journal of molecular and cellular cardiology.

[34]  M. Bernier,et al.  Reperfusion‐induced Arrhythmias and Oxygen‐derived Free Radicals: Studies with “Anti‐Free Radical” Interventions and a Free Radical‐generating System in the Isolated Perfused Rat Heart , 1986, Circulation research.

[35]  R. Lee,et al.  Surfactant-induced sealing of electropermeabilized skeletal muscle membranes in vivo. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[36]  J. Ruskin,et al.  Relation between shock-related myocardial injury and defibrillation efficacy of monophasic and biphasic shocks in a canine model. , 1994, Circulation.

[37]  A. Adgey,et al.  Failure of countershock-type pulses in vitro to adversely alter mitochondrial oxidative phosphorylation. , 1992, Annals of emergency medicine.

[38]  P D Wolf,et al.  Improved defibrillation thresholds with large contoured epicardial electrodes and biphasic waveforms. , 1987, Circulation.

[39]  U. Zimmermann,et al.  The effect of pressure on the electrical breakdown in the membranes of Valonia utricularis. , 1977, Biochimica et biophysica acta.

[40]  S. Rush,et al.  Resistivity of Body Tissues at Low Frequencies , 1963, Circulation research.

[41]  B PELESKA,et al.  Cardiac Arrhythmias Following Condenser Discharges and Their Dependence Upon Strength of Current and Phases of Cardiac Cycle , 1963, Circulation research.

[42]  G. Klein,et al.  Defibrillation shocks increase myocardial pacing threshold: an intracellular microelectrode study. , 1991, The American journal of physiology.

[43]  D Needham,et al.  Electro-mechanical permeabilization of lipid vesicles. Role of membrane tension and compressibility. , 1989, Biophysical journal.

[44]  J. Spear,et al.  The cellular electrophysiologic changes induced by high-energy electrical ablation in canine myocardium. , 1986, Circulation.

[45]  G. Klein,et al.  Changes in pacing threshold and R wave amplitude after transvenous catheter countershock. , 1984, Journal of the American College of Cardiology.

[46]  P D Wolf,et al.  Three‐dimensional Potential Gradient Fields Generated by Intracardiac Catheter and Cutaneous Patch Electrodes , 1992, Circulation.

[47]  E. Wright,et al.  Anode break excitation on single Ranvier node of frog nerve. , 1961, The American journal of physiology.

[48]  G. Christé,et al.  Membrane responses to large hyperpolarizations in trabecles and single cells of frog atrium. , 1988, General physiology and biophysics.

[49]  J. B. Bridges,et al.  Death and damage caused by multiple direct current shocks: studies in an animal model. , 1988, European heart journal.

[50]  G A Ewy,et al.  Myocardial Necrosis from Direct Current Countershock: Effect of Paddle Electrode Size and Time Interval Between Discharges , 1974, Circulation.

[51]  J. Schuder,et al.  Incidence of Arrhythmias in the Dog Following Transthoracic Ventricular Defibrillation with Unidirectional Rectangular Stimuli , 1968, Circulation research.

[52]  L Tung,et al.  Electroporation and recovery of cardiac cell membrane with rectangular voltage pulses. , 1992, The American journal of physiology.

[53]  H Calkins,et al.  Temperature monitoring during radiofrequency catheter ablation of accessory pathways. , 1992, Circulation.

[54]  P. Tchou,et al.  Automatic implantable cardioverter/defibrillator discharges and acute myocardial injury. , 1990, Circulation.

[55]  H. Döring,et al.  Myocardial fiber necrosis due to intracellular Ca overload-a new principle in cardiac pathophysiology. , 1974, Recent advances in studies on cardiac structure and metabolism.

[56]  R E Jones,et al.  Postshock arrhythmias—a possible cause of unsuccessful defibrillation , 1980, Critical care medicine.

[57]  M. R. Tarasevich,et al.  [Electrical breakdown of lipid bilayer membranes]. , 1978, Doklady Akademii nauk SSSR.

[58]  R E Jones,et al.  Microlesion formation in myocardial cells by high-intensity electric field stimulation. , 1987, The American journal of physiology.

[59]  C. Proskauer,et al.  Ultrastructural Injury to Chick Myocardial Cells in Vitro Following "Electric Countershock" , 1980, Circulation research.

[60]  É. Lavallée,et al.  Physical and Dynamic Characteristics of DC Ablation in Relation to the Type of Energy Delivery and Catheter Design , 1991, Pacing and clinical electrophysiology : PACE.

[61]  L. Chernomordik,et al.  Reversible electrical breakdown of lipid bilayers: formation and evolution of pores. , 1988, Biochimica et biophysica acta.

[62]  Y Kim,et al.  Uniformity of current density under stimulating electrodes. , 1990, Critical reviews in biomedical engineering.

[63]  M. Talajic,et al.  Success, Safety, and Late Electrophysiological Outcome of Low‐Energy Direct‐Current Ablation in Patients With the Wolff‐Parkinson‐White Syndrome , 1992, Circulation.

[64]  G. Bardy,et al.  Catheter‐Mediated Electrical Ablation: The Relation Between Current and Pulse Width on Voltage Breakdown and Shock‐wave Generation , 1986, Circulation research.

[65]  J. Crowley,et al.  Electrical breakdown of bimolecular lipid membranes as an electromechanical instability. , 1973, Biophysical journal.

[66]  Y. Chizmadzhev,et al.  Electrical Breakdown of Lipid Bilayer Membranes Phenomenology and Mechanism , 1989 .

[67]  A O Grant,et al.  Asymmetrical electrically induced injury of rabbit ventricular myocytes. , 1995, Journal of molecular and cellular cardiology.

[68]  G. Hutchins,et al.  Pathologic findings related to the lead system and repeated defibrillations in patients with the automatic implantable cardioverter-defibrillator. , 1987, Journal of the American College of Cardiology.

[69]  G. Klein,et al.  Defibrillation shocks produce different effects on Purkinje fibers and ventricular muscle: implications for successful defibrillation, refibrillation and postshock arrhythmia. , 1993, Journal of the American College of Cardiology.

[70]  D. Dimitrov,et al.  Membrane electroporation--fast molecular exchange by electroosmosis. , 1990, Biochimica et biophysica acta.

[71]  E. Boyd,et al.  Bioelectric Effects of High-Energy, Electrical Discharges , 1988 .

[72]  U. Zimmermann,et al.  Electric pulse induced membrane permeabilization. Spatial orientation and kinetics of solute efflux in freely suspended and dielectrophoretically aligned plant mesophyll protoplasts. , 1989, Biochimica et biophysica acta.

[73]  H. Greene,et al.  Effects of High-Energy Electrical Shocks Delivered to the Atrium of the Coronary Sinus , 1988 .

[74]  J. Spear,et al.  Cellular Electrophysiology of Electrical Discharges , 1988 .

[75]  S. Rush,et al.  Local potential gradients as a unifying measure for thresholds of stimulation, standstill, tachyarrhythmia and fibrillation appearing after strong capacitor discharges. , 1978, Advances in cardiology.

[76]  W M Smith,et al.  Prolongation and shortening of action potentials by electrical shocks in frog ventricular muscle. , 1994, The American journal of physiology.

[77]  I. V. Van Gelder,et al.  Incidence and clinical significance of ST segment elevation after electrical cardioversion of atrial fibrillation and atrial flutter. , 1991, American heart journal.

[78]  M. Niebauer,et al.  Efficacy and safety of defibrillation with rectangular waves of 2− to 20‐milliseconds duration , 1983, Critical care medicine.

[79]  S. Rush,et al.  Response of cultured myocardial cells to countershock-type electric field stimulation. , 1978, The American journal of physiology.

[80]  P D Wolf,et al.  Cardiac Potential and Potential Gradient Fields Generated by Single, Combined, and Sequential Shocks During Ventricular Defibrillation , 1992, Circulation.

[81]  Jerry H. Gold,et al.  Transthoracic Ventricular Defibrillation in the 100 kg Calf with Symmetrical One-Cycle Bidirectional Rectangular Wave Stimuli , 1983, IEEE Transactions on Biomedical Engineering.

[82]  J. Jones,et al.  Decreased defibrillator-induced dysfunction with biphasic rectangular waveforms. , 1984, The American journal of physiology.

[83]  R. Hauer,et al.  Electrode catheter ablation for ventricular tachycardia: efficacy of a single cathodal shock. , 1989, British heart journal.

[84]  J. Jones,et al.  Postcountershock fibrillation in digitalized myocardial cells in vitro , 1980, Critical care medicine.

[85]  D. Haines,et al.  Cellular Electrophysiological Effects of Hyperthermia on Isolated Guinea Pig Papillary Muscle Implications for Catheter Ablation , 1993, Circulation.

[86]  R E Ideker,et al.  Shock Strength for the Implantable Defibrillator: Can You Have Too Much of a Good Thing? , 1992, Pacing and clinical electrophysiology : PACE.

[87]  R. Stampflj,et al.  Reversible electrical breakdown of the excitable membrane of a Ranvier node , 1958 .

[88]  L. Tung,et al.  Comparison of electroporation thresholds of cardiac cell membranes by rectangular and exponential pulses , 1995, Proceedings of 17th International Conference of the Engineering in Medicine and Biology Society.

[89]  H. Rogove,et al.  Defibrillation and cardioversion. , 1992, Critical care clinics.

[90]  D. Haines,et al.  Observations on electrode-tissue interface temperature and effect on electrical impedance during radiofrequency ablation of ventricular myocardium. , 1990, Circulation.

[91]  J. Cohn,et al.  Myocardial damage after repetitive direct current shock in the dog: correlation between left ventricular end-diastolic pressure and extent of myocardial necrosis. , 1978, The Journal of laboratory and clinical medicine.

[92]  R. Kernoff,et al.  Cardiac damage produced by direct current countershock applied to the heart. , 1979, The American journal of cardiology.

[93]  L Tung,et al.  Electroporation of Cardiac Cell Membranes with Monophasic or Biphasic Rectangular Pulses , 1991, Pacing and clinical electrophysiology : PACE.

[94]  G. Wagner,et al.  Cardiac Inotropic and Coronary Vascular Responses to Countershock: Evidence For Excitation Of Intracardiac Nerves , 1968, Circulation research.

[95]  L. Opie,et al.  Reperfusion damage: free radicals mediate delayed membrane changes rather than early ventricular arrhythmias. , 1990, Cardiovascular research.

[96]  G. Saulis,et al.  Kinetics of pore resealing in cell membranes after electroporation , 1991 .

[97]  L. J. Fogelson,et al.  Electrophysiologic depression in myocardium by defibrillation-level shocks , 1988, Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[98]  L Tung,et al.  Spatial distribution of cardiac transmembrane potentials around an extracellular electrode: dependence on fiber orientation. , 1995, Biophysical journal.

[99]  H. Schneider,et al.  Cardiac damage caused by direct application of defibrillator shocks to isolated Langendorff-perfused rabbit heart. , 1980, American heart journal.

[100]  W. Weglicki,et al.  Abnormal electrical activity induced by free radical generating systems in isolated cardiocytes. , 1988, Journal of molecular and cellular cardiology.