Abstract
Temperature plays an important role in the electrophysiology of cardiomyocytes. Pulmonary veins (PVs) are known to initiate paroxysmal atrial fibrillation. The effects of temperature on the arrhythmogenic activity of rabbit single PV and atrial cardiomyocytes were assessed using the whole-cell clamp technique. PV cardiomyocytes had different beating rates at low (22–25°C), normal (38–39°C) and high (40–41°C) temperatures (0.9±0.1, 3.2±0.4, 6.4±0.6 Hz, respectively; p<0.001). There were different action potential durations and incidences of delayed afterdepolarization in PV cardiomyocytes with pacemaker activity (31, 59, 63%; p<0.05), PV cardiomyocytes without pacemaker activity (16, 47, 60%; p<0.001), and atrial myocytes (0, 0, 21%; p<0.05). However, oscillatory afterpotentials were only found in PV cardiomyocytes with pacemaker activity at normal (50%) or high (68%) temperatures, but not at low temperatures (p<0.001). Both PV and atrial cardiomyocytes had larger transient inward currents and inward rectified currents at high temperatures. Additionally, PV cardiomyocytes with and without pacemaker activity had larger pacemaker currents at higher temperatures. This study demonstrated that PV cardiomyocytes have an increase in arrhythmogenic activity at high temperatures because of enhanced automaticity, induced triggered activity, or shortening of action potential duration.
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Bjornstad H, Tande PM, Lathrop DA, Refsum H. Effects of temperature on cycle length dependent changes and restitution of action potential duration in guinea pig ventricular muscle. Cardiovasc Res 27:946–950;1993.
Bolter CP, Atkinson KJ. Influence of temperature and adrenergic stimulation on rat sinoatrial frequency. Am J Physiol 254:R840-R844;1988.
Cranefield PF. Action potentials, afterpotentials, and arrhythmias. Circ Res 41:415–23;1977.
Cavalie A, McDonald TF, Pelzer D, Trautwein W. Temperature-induced transitory and steady-state changes in the calcium current of guinea pig ventricular myocytes. Pflügers Arch 405:294–296;1985.
Cerbai E, Pino R, Porciatti F, Sani G, Toscano M, Maccherini M, Giunti G, Mugelli A. Characterization of the hyperpolarization-activated current, If, in ventricular myocytes from human failing heart. Circulation 95:568–571;1997.
Chen YC, Chen SA, Chen YJ, Chang MS, Chan P, Lin CI. Effects of thyroid hormone on the arrhythmogenic activity of pulmonary veins cardiomyocytes. J Am Coll Cardiol 39:366–372;2002.
Chen YJ, Chen SA, Chang MS, Lin CI. Arrhythmogenic activity of cardiac muscle in pulmonary veins of the dog: Implication for the genesis of atrial fibrillation. Cardiovasc Res 48:265–273;2000.
Chen YJ, Chen SA, Chen YC, Yeh HI, Chan P, Chang MS, Lin CI. Effects of rapid atrial pacing on the arrhythmogenic activity of single cardiomyocytes from pulmonary veins: Implication in initiation of atrial fibrillation. Circulation 104:2849–2854;2001.
Chen YJ, Chen SA, Chen YC, Yeh HI, Chang MS, Lin CI. Electrophysiology of single cardiomyocytes isolated from rabbit pulmonary veins: Implication in initiation of focal atrial fibrillation. Basic Res Cardiol 97:26–34;2002.
Chen SA, Hsieh MH, Tai CT, Tsai CF, Prakash VS, Yu WC, Hsu TL, Ding YA, Chang MS. Initiation of atrial fibrillation by ectopic beats originating from the pulmonary veins: Electrophysiological characteristics, pharmacological responses, and effects of radiofrequency ablation. Circulation 100:1879–1886;1999.
DiFrancesco D. The onset and autonomic regulation of cardiac pacemaker activity: Relevance of the F currents. Cardiovasc Res 29:449–456;1995.
Dumaine R, Towbin JA, Brugada P, Vatta M, Nesterenko DV, Nesterenko VV, Brugada J, Brugada R, Antzelevitch C. Ionic mechanisms responsible for the electrocardiographic phenotype of the Brugada syndrome are temperature dependent. Circ Res 85:803–809;1999.
Haissaguerre M, Jais P, Shah DC, Takahashi A, Hocini M, Quiniou G, Garrigue S, Le Mouroux A, Le Metayer P, Clementy J. Spontaneous initiation of atrial fibrillation by ectopic beats originating in the pulmonary veins. N Engl J Med 339:659–666;1998.
Kirsch GE, Sykes JS. Temperature dependence of Na currents in rabbit and frog muscle membranes. J Gen Physiol 89:239–251;1987.
Kiyosue T, Arita M, Muramatsue H, Spindler AJ, Noble D. Ionic mechanisms of action potential prolongation at low temperature in guinea-pig ventricular myocytes. J Physiol (Lond) 468:85–106;1993.
Kobayashi M, Godin D, Nadeau R. Sinus node response to perfusion pressure changes, ischemia and hypothermia in the isolated blood-perfused dog atrium. Cardiovasc Res 19:20–26;1985.
Masani F. Node-like cells in the myocardial layer of the pulmonary vein of rats: An ultrastructural study. J Anat 145:133–142;1986.
Mugelli A, Cerbai E, Amerini S, Visentin S. The role of temperature on the development of oscillatory afterpotentials and triggered activity. J Mol Cell Cardiol 18:1313–1316;1986.
Nathan H, Eliakim M. The junction between the left atrium and the pulmonary veins: An anatomic study of human hearts. Circulation 34:412–422;1966.
Ng GA, Lau EW, Griffith MJ. Temperature-sensitive focal atrial tachycardia in the left atrium. J Cardiovasc Electrophysiol 11:324–327;2000.
Noma A, Nakayama T, Kurachi Y, Irisawa H. Resting K conductances in pacemaker and non-pacemaker heart cells of the rabbit. Jpn J Physiol 34:245–254;1984.
Pfammatter JP, Paul T, Ziemer G, Kallfelz HC. Successful management of junctional tachycardia by hypothermia after cardiac operations in infants. Ann Thorac Surg 60:556–560;1995.
Saito T, Waki K, Becker AE. Left atrial myocardial extension onto pulmonary veins in humans: Anatomic observations relevant for atrial arrhythmias. J Cardiovasc Electrophysiol 11:888–894;2000.
Satoh H, Sperelakis N. Hyperpolarization-activated inward current in embryonic chick cardiac myocytes: Developmental changes and modulation by isoproterenol and carbachol. Eur J Pharmacol 240:283–290;1993.
Spear JF, Moore EN. Modulation of quinidine-induced arrhythmias by temperature in perfused rabbit heart. Am J Physiol 43:H817-H828;1998.
Tseng GN, Wit AL. Characteristics of a transient inward current that causes delayed after-depolarizations in atrial cells of canine coronary sinus. J Mol Cell Cardiol 19:1105–1119;1987.
Walsh EP, Saul JP, Hulse JE, Rhodes LA, Hordof AJ, Mayer JE, Lock JE. Transcatheter ablation of ectopic atrial tachycardia in young patients using radiofrequency current. Circulation 86:1138–1146;1992.
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Chen, YJ., Chen, YC., Chan, P. et al. Temperature regulates the arrhythmogenic activity of pulmonary vein cardiomyocytes. J Biomed Sci 10, 535–543 (2003). https://doi.org/10.1007/BF02256115
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DOI: https://doi.org/10.1007/BF02256115