Cardiac arrhythmia mechanisms in rats with heart failure induced by pulmonary hypertension

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 11, 2012, Pages

  Benoist, David ^a,b   Stones, Rachel ^a   Drinkhill, Mark J ^a   Benson, Alan P ^a   Yang, Zhaokang ^a   Cassan, Cecile ^c   Gilbert, Stephen H ^a,b   Saint, David A ^d   Cazorla, Olivier ^c   Steele, Derek S ^a   Rernus, Olivier ^a,b   White, Ed ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b CENTRE DE RECHERCHE CARDIO THORACIQUE DE BORDEAUX   (France)

^c INSERM   (France)

^d UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Alternans; Calcium signaling; Electrocardiography; Monocrotaline; Voltage sensitive dye imaging

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CONSCIOUSNESS; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; ELECTRIC ACTIVITY; ELECTROCARDIOGRAM; ENZYME ACTIVITY; HEART ARRHYTHMIA; HEART MUSCLE CELL; HEART RIGHT VENTRICLE FAILURE; HEART RIGHT VENTRICLE HYPERTROPHY; ISOLATED HEART; MALE; NONHUMAN; PRIORITY JOURNAL; PULMONARY HYPERTENSION; RAT; SARCOPLASMIC RETICULUM; SUDDEN DEATH; T WAVE; TELEMETRY;

ACTION POTENTIALS; ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM; CALCIUM-TRANSPORTING ATPASES; ELECTROCARDIOGRAPHY; HEART FAILURE; HYPERTENSION, PULMONARY; MALE; MODELS, ANIMAL; MYOCYTES, CARDIAC; RATS; RATS, WISTAR; SARCOPLASMIC RETICULUM; VENTRICULAR DYSFUNCTION, RIGHT;

EID: 84861790477     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01084.2011     Document Type: Article

References (63)

1. Antzelevitch C. Role of spatial dispersion of repolarization in inherited and acquired sudden cardiac death syndromes. Am J Physiol Heart Circ Phvsiol 293: H2024-H2038. 2007.
2. Antzelevitch C, Sicouri S, Di Diego JM, Burashnikov A, Viskin S, Shimizu W, Yan GX, Kowey P, Zhang L. Does Tpeak-Tend provide an index of transmural dispersion of repolarization? Heart Rhythm 4: 1114- 1116, 2007.
3. Benoist D, Stones R, Drinkhill M, Bernus O, White E. Arrhythmogenic substrate in hearts of rats with monocrotaline-induced pulmonary hypertension and right ventricular hypertrophy. Am J Physiol Heart Circ Physiol 300: H2230-H2237, 2011.
4. Benson AP, Gilbert SH, Li P, Newton SM, Holden AV. Reconstruction and quantification of diffusion tensor imaging-derived cardiac fibre and sheet structure in ventricular regions used in studies of excitation propagation. Math Model Nat Phenom 3: 101-130, 2008.
5. + in normal and failing cardiac myocytes. Ann NY Acad Sci 1080: 165-177, 2006.
6. Bogaard HJ, Abe K, Vonk NA, Voelkel NF. The right ventricle under pressure: cellular and molecular mechanisms of right-heart failure in pulmonary hypertension. Chest 135: 794-804, 2009.
7. Bovill JG. Intravenous anesthesia for the patient with left ventricular dysfunction. Semin Cardiothorac Vasc Anesth 10: 43-48, 2006.
8. Cheng H, Lederer WJ. Calcium sparks. Physiol Rev 88: 1491-1545, 2008.
9. Cutler MJ, Rosenbaum DS. Explaining the clinical manifestations of T wave alternans in patients at risk for sudden cardiac death. Heart Rhythm 6: S22-S28, 2009.
10. D'Alonzo GE, Barst RJ, Ayres SM, Bergofsky EH, Brundage BH, Detre KM, Fishman AP, Goldring RM, Groves BM, Kernis JT. Survival in patients with primary pulmonary hypertension. Results from a national prospective registry. Ann Intern Med 115: 343-349, 1991.
11. de Simone G, Wallerson DC, Volpe M, Devereux RB. Echocardiographic measurement of left ventricular mass and volume in normotensive and hypertensive rats. Necropsy validation. Am J Hypertens 3: 688-696, 1990.
12. 2+ in cardiac hypertrophy. Cardiovasc Res 62: 538-547, 2004.
13. Diaz ME, O'Neill S., Eisner DA. Sarcoplasmic reticulum calcium content fluctuation is the key to cardiac alternans. Circ Res 94: 650-656, 2004.
14. 2+]i. J Physiol 585: 579-592, 2007.
15. Endo H, Miura M, Hirose M, Takahashi J, Nakano M, Wakayama Y, Sugai Y, Kagaya Y, Watanabe J, Shirato K, Shimokawa H. Reduced inotropic effect of nifekalant in failing hearts in rats. J Pharmacol Exp Ther 318: 1102-1107, 2006.
16. Engelman ZJ, Trew ML, Smaill BH. Structural heterogeneity alone is a sufficient substrate for dynamic instability and altered restitution. Circ Arrhythm Electrophysiol 3: 195-203, 2010.
17. Folino AF, Bobbo F, Schiraldi C, Tona F, Romano S, Buja G, Bellotto F. Ventricular arrhythmias and autonomic profile in patients with primary pulmonary hypertension. Lung 181: 321-328, 2003.
18. Haddad F, Doyle R, Murphy DJ, Hunt SA. Right ventricular function in cardiovascular disease, part II: pathophysiology, clinical importance, and management of right ventricular failure. Circulation 117: 1717-1731, 2008.
19. Handoko ML, de Man FS, Allaart CP, Paulus WJ, Westerhof N, Vonk-Noordegraaf A. Perspectives on novel therapeutic strategies for right heart failure in pulmonary arterial hypertension: lessons from the left heart. Eur Respir Rev 19: 72-82, 2010.
20. Handoko ML, de Man FS, Happe CM, Schalij I, Musters RJ, Westerhof N, Postmus PE, Paulus WJ, van der Laarse WJ, Vonk-Noordegraaf A. Opposite effects of training in rats with stable and progressive pulmonary hypertension. Circulation 120: 42-49, 2009.
21. Hardziyenka M, Campian ME, de Bruin-Bon HA, Michel MC, Tan HL. Sequence of echocardiographic changes during development of right ventricular failure in rat. J Am Soc Echocardiogr 19: 1272-1279, 2006.
22. Henkens IR, Mouchaers KT, Vliegen HW, van der Laarse WJ, Swenne CA, Maan AC, Draisma HH, Schalij I, van der Wall EE, Schalij MJ, Vonk-Noordegraaf A. Early changes in rat hearts with developing pulmonary arterial hypertension can be detected with three-dimensional electrocardiography. Am J Physiol Heart Circ Physiol 293: H1300-H1307, 2007.
23. Henkens IR, Mouchaers KT, Vonk-Noordegraaf A, Boonstra A, Swenne CA, Maan AC, Man SC, Twisk JW, van der Wall EE, Schalij MJ, Vliegen HW. Improved ECG detection of presence and severity of right ventricular pressure load validated with cardiac magnetic resonance imaging. An J Physiol Heart Circ Physiol 294: H2150-H2157, 2008.
24. Hessel MH, Steendijk P, den Adel B, Schutte CI, van der Laarse A. Characterization of right ventricular function after monocrotaline-induced pulmonary hypertension in the intact rat. Am J Physiol Heart Circ Physiol 291: H2424-H2430, 2006.
25. 2+ spark mass. J Mol Cell Cardiol 48: 293-301. 2010.
26. Hlaing T, Guo D, Zhao X, DiMino T, Greenspon L, Kowey PR, Yan GX. The QT and Tp-e intervals in left and right chest leads: comparison between patients with systemic and pulmonary hypertension. J Electrocardiol 38: 154-158, 2005.
27. Hong-liang Z, Qin L, Zhi-hong L, Zhi-hui Z, Chang-ming X, Xin-hai N, Jian-guo H, Ying-jie W, Shu Z. Heart rate-corrected QT interval and QT dispersion in patients with pulmonary hypertension. Wien Klin Wochenschr 121: 330-333, 2009.
28. Houser SR, Margulies KB. Is depressed myocyte contractility centrally involved in heart failure? Circ Res 92: 350-358, 2003.
29. Hyatt CJ, Zemlin CW, Smith RM, Matiukas A, Pertsov AM, Bernus O. Reconstructing subsurface electrical wave orientation from cardiac epi-fluorescence recordings: Monte Carlo versus diffusion approximation. Opt Express 16: 13758-13772, 2008.
30. Jones JE, Mendes L, Rudd MA, Russo G, Loscalzo J, Zhang YY. Serial noninvasive assessment of progressive pulmonary hypertension in a rat model. Am J Physiol Heart Circ Physiol 283: H364-H371, 2002.
31. Kawara T, Derksen R, de Groot JR, Coronel R, Tasseron S, Linnenbank AC, Hauer RN, Kirkels H, Janse MJ, de Bakker JM. Activation delay after premature stimulation in chronically diseased human myocardium relates to the architecture of interstitial fibrosis. Circulation 104: 3069-3075, 2001.
32. Keldermann RH, Ten Tusscher KH, Nash MP, Hren R, Taggart P, Panfilov AV. Effect of heterogeneous APD restitution on VF organization in a model of the human ventricles. Ant J Physiol Heart Circ Physiol 294: H764-H774, 2008.
33. Kogler H, Hartmann O, Leineweber K, Nguyen vP, Schott P, Brodde OE, Hasenfuss G. Mechanical load-dependent regulation of gene expression in monocrotaline-induced right ventricular hypertrophy in the rat. Circ Res 93: 230-237, 2003.
34. Kondo RP, Dederko DA, Teutsch C, Chrast J, Catalucci D, Chien KR, Giles WR. Comparison of contraction and calcium handling between right and left ventricular myocytes from adult mouse heart: a role for repolarization waveform. J Physiol 571: 131-146, 2006.
35. Laurita KR, Rosenbaum DS. Cellular mechanisms of arrhythmogenic cardiac alternans. Prog Biophys Mol Biol 97: 332-347, 2008.
36. Lee JK, Kodama I, Honjo H, Anno T, Kamiya K, Toyama J. Stage-dependent changes in membrane currents in rats with monocrotaline-induced right ventricular hypertrophy. Am J Physiol Heart Circ Physiol 272: H2833-H2842, 1997.
37. + channels in rat heart with right ventricular hypertrophy. Am J Physiol Heart Circ Physiol 277: H1725-H1731, 1999.
38. 2+ alternans in rat ventricular myocytes. J Physiol 587: 1283-1292, 2009.
39. Lou Q, Li W, Efimov IR. The role of dynamic instability and wavelength in arrhythmia maintenance as revealed by panoramic imaging with blebbistatin vs. 2,3-butanedione monoxime. Am J Physiol Heart Circ Physiol 302: H262-H269, 2012.
40. McCrossan ZA, Billeter R, White E. Transmural changes in size, contractile and electrical properties of SHR left ventricular myocytes during compensated hypertrophy. Cardiovasc Res 63: 283-292, 2004.
41. Meyer BL, Bogart DB, Carley JE, Wong BY, Dunn MI. Pulmonary arterial pulsus alternans secondary to primary pulmonary hypertension. Chest 70: 374-377, 1976.
42. 2+ transients in mice during early congestive heart failure. J Mol Cell Cardiol 43: 177-186, 2007.
43. Myles RC, Burton FL, Cobbe SM, Smith GL. Alternans of action potential duration and amplitude in rabbits with left ventricular dysfunction following myocardial infarction. J Mol Cell Cardiol 50: 510-521, 2011.
44. Opthof T, Coronel R, Wilms-Schopman FJ, Plotnikov AN, Shlapakova IN, Danilo P Jr, Rosen MR, Janse MJ. Dispersion of repolarization in canine ventricle and the electrocardiographic T wave: Tp-e interval does not reflect transmural dispersion. Heart Rhythm 4: 341-348, 2007.
45. Papadakis NG, Xing D, Huang CL, Hall LD, Carpenter TA. A comparative study of acquisition schemes for diffusion tensor imaging using MRI. J Magn Reson 137: 67-82, 1999.
46. Piacentino V, III, Weber CR, Chen X, Weisser-Thomas J, Marguties KB, Bers DM, Houser SR. Cellular basis of abnormal calcium transients of failing human ventricular myocytes. Circ Res 92: 651-658, 2003.
47. Piao L, Fang YH, Cadete VJ, Wietholt C, Urboniene D, Toth PT, Marsboom G, Zhang HJ, Haber I, Rehman J, Lopaschuk GD, Archer SL. The inhibition of pyruvate dehydrogenase kinase improves impaired cardiac function and electrical remodeling in two models of right ventricular hypertrophy: resuscitating the hibernating right ventricle. J Mol Med 88: 47-60. 2010.
48. Picht E, DeSantiago J, Blatter LA, Bers DM. Cardiac alternans do not rely on diastolic sarcoplasmic reticulum calcium content fluctuations. Circ Res 99: 740-748, 2006.
49. Qu Z, Xie Y, Garfinkel A, Weiss JN. T-wave alternans and arrhythmogenesis in cardiac diseases. Front Physiol 1: 154, 2010.
50. Sahn DJ, DeMaria A, Kisslo J, Weyman A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58: 1072-1083, 1978.
51. Sanyal SN, Ono K. Derangement of autonomic nerve control in rat with right ventricular failure. Pathophysiology 8: 197-203, 2002.
52. Scollan DF, Holmes A, Winslow R, Forder J. Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am J Physiol Heart Circ Physiol 275: H2308-H2318, 1998.
53. Selvaraj RJ, Picton P, Nanthakumar K, Chauhan VS. Steeper restitution slopes across right ventricular endocardium in patients with cardiomyopathy at high risk of ventricular arrhythmias. Am J Physiol Heart Circ Physiol 292: H1262-H1268, 2007.
54. Slama M, Susic D, Varagic J, Ahn J, Frohlich ED. Echocardiographic measurement of cardiac output in rats. Am J Physiol Heart Circ Physiol 284: H691-H697, 2003.
55. Takebayashi S, Li Y, Kaku T, Inagaki S, Hashimoto Y, Kimura K, Miyamoto S, Hadama T, Ono K. Remodeling excitation-contraction coupling of hypertrophied ventricular myocytes is dependent on T-type calcium channels expression. Biochem Biophys Res Commun 345: 766-773, 2006.
56. Umar S, Lee JH, de LE, Iorga A, Partow-Navid R, Bapat A, van der LA, Saggar R, Saggar R, Ypey DL, Karagueuzian HS, Eghbali M. Spontaneous ventricular fibrillation in right ventricular failure secondary to chronic pulmonary hypertension. Circ Arrhythm Electrophysiol 5: 181-190, 2012.
57. Uzzaman M, Honjo H, Takagishi Y, Emdad L, Magee AI, Severs NJ, Kodama I. Remodeling of gap junctional coupling in hypertrophied right ventricles of rats with monocrotaline-induced pulmonary hypertension. Circ Res 86: 871-878, 2000.
58. Voelkel NF, Quaife RA, Leinwand LA, Barst RJ, McGoon MD, Meldrum DR, Dupuis J, Long CS, Rubin LJ, Smart FW, Suzuki YJ, Gladwin M, Denholm EM, Gail DB. Right ventricular function and failure: report of a National Heart, Lung, and Blood Institute working group on cellular and molecular mechanisms of right heart failure. Circulation 114: 1883-1891. 2006.
59. Walton RD, Benoist D, Hyatt CJ, Gilbert SH, White E, Bernus O. Dual excitation wavelength epifluorescence imaging of transmural electrophysiological properties in intact hearts. Heart Rhythm 7: 1843-1849, 2010.
60. Weiss JN, Nivala M, Garfinkel A, Qu Z. Alternans and arrhythmias: from cell to heart. Circ Res 108: 98-112, 2011.
61. 2+ release in permeabilized cardiomyocytes. Cardiovasc Res 70: 475-485, 2006.
62. 2+ content in permeabilized cardiac myocytes. Circ Res 89: 526-533, 2001.
63. Zipes DP, Camm AJ, Borggrefe M, Buxton AE, Chaitman B, Fromer M, Gregoratos G, Klein G, Moss AJ, Myerburg RJ, Priori SG, Quinones MA, Roden DM, Silka MJ, Tracy C, Smith SC Jr, Jacobs AK, Adams CD, Antman EM, Anderson JL, Hunt SA, Halperin JL, Nishimura R, Ornato JP, Page RL, Riegel B, Blanc JJ, Budaj A, Dean V, Deckers JW, Despres C, Dickstein K, Lekakis J, McGregor K, Metra M, Morais J, Osterspey A, Tamargo JL, Zamorano JL. ACC/ AHA/ESC 2006 Guidelines for Management of Patients With Ventricular Arrhythmias and the Prevention of Sudden Cardiac Death: a report of the American College of Cardiology/American Heart Association Task Force and the European Society of Cardiology Committee for Practice Guidelines (writing committee to develop Guidelines for Management of Patients With Ventricular Arrhythmias and the Prevention of Sudden Cardiac Death): developed in collaboration with the European Heart Rhythm Association and the Heart Rhythm Society. Circulation 114: e385-e484, 2006.