Influence of I Ks heterogeneities on the genesis of the T-wave: A computational evaluation

IEEE Transactions on Biomedical Engineering

Volumn 59, Issue 2, 2012, Pages 311-322

  Keller, David U J ^a   Weiss, Daniel L ^b   Dossel, Olaf ^a   Seemann, Gunnar ^b  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b Sirona Dental Systems GmbH   (Germany)

Author keywords

Computational evaluation; dispersion of repolarization (DOR); electrophysiological heterogeneities; T wave

Indexed keywords

ACTION POTENTIAL DURATIONS; ACTIVATION TIME; BEST MATCH; BIVENTRICULAR MODELS; CARDIAC ACTIVATION; COMPUTATIONAL EVALUATION; ECG DATA; ELECTROPHYSIOLOGICAL HETEROGENEITIES; HIGH RESOLUTION; ION CHANNEL; LOW-AMPLITUDE; MULTI-CHANNEL; QUANTITATIVE EVALUATION; REPOLARIZATION; T WAVES; T-WAVE; TRANSMEMBRANE VOLTAGE;

COMPUTER SIMULATION; ELECTROCARDIOGRAPHY; ELECTROPHYSIOLOGY; MORPHOLOGY;

DISPERSION (WAVES);

ION CHANNEL;

ACTION POTENTIAL; ANISOTROPY; ARTICLE; ELECTRIC CURRENT; ELECTRIC POTENTIAL; HEART REPOLARIZATION; HEART VENTRICLE; MATHEMATICAL ANALYSIS; MODEL; T WAVE;

ANIMALS; COMPUTER SIMULATION; DOGS; ELECTROCARDIOGRAPHY; GUINEA PIGS; HEART; HEART CONDUCTION SYSTEM; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, CARDIOVASCULAR; RABBITS; SIGNAL PROCESSING, COMPUTER-ASSISTED; SWINE;

EID: 84856153815     PISSN: 00189294     EISSN: 15582531     Source Type: Journal    
DOI: 10.1109/TBME.2011.2168397     Document Type: Article

References (85)

1. F. L. Burton and S. M. Cobbe, "Dispersion of ventricular repolarization and refractory period," Cardiovasc. Res., vol. 50, pp. 1-23, 2001.
2. J. M. T. de Bakker and T. Opthof, "Is the apico-basal gradient larger than the transmural gradient?" J. Cardiovasc. Pharm., vol. 39, pp. 328-331, 2002.
3. Y. Pereon, S. Demolombe, I. Baro, E. Drouin, F. Charpentier, and D. Escande, "Differential expression of KvLQT1 isoforms across the human ventricular wall," Amer. J. Physiol. Heart Circ. Physiol., vol. 278, pp. 1908-1915, 2000.
4. D. Noble and I. Cohen, "The interpretation of the T wave of the electrocardiogram," Cardiovasc. Res., vol. 12, pp. 13-27, 1978.
5. A. V. Glukhov, V. V. Fedorov, Q. Lou, V. K. Ravikumar, P. W. Kalish, R. B. Schuessler, N. Moazami, and I. R. Efimov, "Transmural dispersion of repolarization in failing and nonfailing human ventricle," Circ. Res., vol. 106, pp. 981-991, 2010.
6. K. Harumi, M. J. Burgess, and J. A. Abildskov, "A theoretic model of the t wave," Circulation, vol. 34, pp. 657-668, 1966.
7. W. T. Miller and D. B. Geselowitz, "Simulation studies of the electrocardiogram. I. The normal heart," Circ. Res., vol. 43, pp. 301-315, 1986.
8. D. di Bernardo and A. Murray, "Computer model for study of cardiac repolarization," J. Cardiovasc. Electr., vol. 11, pp. 895-899, 2000.
9. J. Xue, Y. Chen, X. Han, and W. Gao, "Electrocardiographic morphology changes with different type of repolarization dispersions," J. Electrocardiol., vol. 43, pp. 553-559, 2010.
10. M. Potse, A. R. LeBlanc, and A. Vinet, "Why do we need supercomputers to understand the electrocardiographic T wave?," Anadolu Kardiyol. Dergisi, vol. 7, pp. 123-124, 2007.
11. P. Viswanathan, R.M. Shaw, and Y. Rudy, "Effects of IKr and IKs heterogeneity on action potential duration and its rate dependence: A simulation study," Circulation, vol. 99, pp. 2466-2474, 1999.
12. K. Gima and Y. Rudy, "Ionic current basis of electrocardiographic waveforms. A model study," Circ. Res., vol. 90, pp. 889-896, 2002.
13. C. E. Conrath, R. Wilders, R. Coronel, J. M. de Bakker, P. Taggart, J. R. de Groot, and T. Opthof, "Intercellular coupling through gap junctions masks Mcells in the human heart," Cardiovasc. Res., vol. 62, pp. 407-414, 2004.
14. P. Colli Franzone, L. F. Pavarino, S. Scacchi, and B. Taccardi, "T wave polarity of simulated electrocardiograms: Influence of transmural heterogeneity," Int. J. Bioelectromagn., vol. 11, pp. 11-16, 2009.
15. M. Potse, B. Dubé, J. Richter, A. Vinet, and R. M. Gulrajani, "A comparison of monodomain and bidomain reaction-diffusion models for action potential propagation in the human heart," IEEE Trans. Biomed. Eng., vol. 53, no. 12, pp. 2425-2435, Dec. 2006.
16. K. J. Sampson and C. S. Henriquez, "Electrotonic influences on action potential duration dispersion in small hearts: A simulation study," Amer. J. Physiol. Heart Circ. Physiol., vol. 289, pp. H350-H360, 2005.
17. M. Potse, A. Vinet, T. Opthof, and R. Coronel, "Validation of a simple model for the morphology of the T wave in unipolar electrograms," Amer. J. Physiol. Heart Circ. Physiol., vol. 297, pp. H792-H801, 2009.
18. P. Colli Franzone, L. F. Pavarino, S. Scacchi, and B. Taccardi, "Modeling ventricular repolarization: Effects of transmural and apex-to-base heterogeneities in action potential durations," Math. Biosci., vol. 214, pp. 140-152, 2008.
19. D. U. J. Keller, O. Jarrousse, T. Fritz, S. Ley, O. Dössel, and G. Seemann, "Impact of physiological ventricular deformation on the morphology of the T-wave: A hybrid, static-dynamic approach," IEEE Trans. Biomed. Eng., vol. 58, no. 7, pp. 2109-2119, Jul. 2011.
20. D. Streeter, "Gross morphology and fiber geometry of the heart," in Handbook of Physiology. Section 2: The Cardiovascular System, Vol. I. The Heart. Baltimore, MD: Williams and Wilkins (Amer. Physiol. Soc.), 1979, pp. 61-112.
21. CGAL, Computational Geometry Algorithms Library. (2011). [Online]. Available: http://www.cgal.org
22. K. H.W. J. ten Tusscher and A. V. Panfilov, "Alternans and spiral breakup in a human ventricular tissue model," Amer. J. Physiol. Heart Circ. Physiol., vol. 291, pp. H1088-H1100, 2006.
23. S. Rush and H. Larsen, "A practical algorithm for solving dynamic membrane equations," IEEE Trans. Biomed. Eng., vol.BME-25, no. 4, pp. 389-392, Jul. 1978.
24. D. U. J. Keller, R. Kalayciyan, O. Dössel, and G. Seemann, "Fast creation of endocardial stimulation profiles for the realistic simulation of body surface ECGs," in Proc. IFMBE, 2009, pp. 145-148.
25. E. Drouin, F. Charpentier, C. Gauthier, K. Laurent, and H. L. Marec, "Electrophysiological characteristics of cells spanning the left ventricular wall of human heart: Evidence for the presence ofMcells," J. Amer. Coll. Cardiol., vol. 26, pp. 185-192, 1995.
26. G. R. Li, J. Feng, L. Yue, and M. Carrier, "Transmural heterogeneity of action potentials and Ito1 in myocytes isolated from the human right ventricle," Amer. J. Physiol., vol. 275, pp. 369-377, 1998.
27. S. Sicouri and C. Antzelevitch, "Distribution of M cells in the canine ventricle," J. Cardiovasc. Electr., vol. 5, pp. 824-837, 1994.
28. G. X. Yan, W. Shimizu, and C. Antzelevitch, "Characteristics and distribution of M cells in arterially perfused canine left ventricular wedge preparations," Circulation, vol. 98, pp. 1921-1927, 1998.
29. S. Sicouri and C. Antzelevitch, "A subpopulation of cells with unique electrophysiological properties in the deep subepicardium of the canine ventricle: The {M} cell," Circ. Res., vol. 68, pp. 1729-1741, 1991.
30. S. Sicouri, A. Glass, M. Ferreiro, and C. Antzelevitch, "Transseptal dispersion of repolarization and its role in the development of Torsade de Pointes arrhythmias," J. Cardiovasc. Electr., vol. 21, pp. 441-447, 2010.
31. F. G. Akar and D. S. Rosenbaum, "Transmural electrophysiological heterogeneities underlying arrhythmogenesis in heart failure," Circ. Res., vol. 93, pp. 638-645, 2003.
32. F. G. Akar, G. X. Yan, C. Antzelevitch, and D. S. Rosenbaum, "Unique topographical distribution of Mcells underlies reentrantmechanism of torsade de pointes in the long-QT sydrome," Circulation, vol. 105, pp. 1247-1253, 2002.
33. E. P. Anyukhovsky, E.A. Sosunov, and M.R. Rosen, "Regional differences in electrophysiological properties of epicardium, midmyocardium, and endocardium," Circulation, vol. 94, pp. 1981-1988, 1996.
34. T. Stankovicova, M. Szilard, I. Scheerder, and K. Sipido, "M cells and transmural heterogeneity of action potential configuration in myocytes from the left ventricular wall of the pig heart," Cardiovasc. Res., vol. 45, pp. 952-960, 2000.
35. S. Sicouri, M. Quist, and C. Antzelevitch, "Evidence for the presence of m cells in the guinea pig ventricle," J. Cardiovasc. Electr., vol. 7, pp. 503-511, 1996.
36. M. A. McIntosh, S. M. Cobbe, and G. L. Smith, "Heterogeneous changes in action potential and intracellular {Ca2+} in left ventricular myocyte subtypes from rabbits with heart failure," Cardiovasc. Res., vol. 45, pp. 397-409, 2000.
37. M. Näbauer, D. J. Beuckelmann, P. Überfuhr, and G. Steinbeck, "Regional differences in current density and rate-dependent properties of the transient outward current in subepicardial and subendocardial myocytes of human left ventricle," Circulation, vol. 93, pp. 168-177, 1996.
38. G. Szabo, N. Szentandrassy, T. Biro, B. I. Toth, G. Czifra, J. Magyar, T. Banyasz, A. Varro, L. Kovacs, and P. P. Nanasi, "Asymmetrical distribution of ion channels in canine and human left-ventricular wall: epicardium versus midmyocardium," Pflugers. Arch., vol. 450, pp. 307-316, 2005.
39. S. Sekiya, S. Ichikawa, T. Tsutsumi, and K. Harumi, "Distribution of action potential durations in the canine left ventricle," Jpn. Heart J., vol. 25, pp. 181-194, 1984.
40. M. N. Obreztchikova, K. W. Patberg, A. N. Plotnikov, N. Ozgen, I. N. Shlapakova, A. V. Rybin, E. A. Sosunov, P. J. Danilo, E. P. Anyukhovsky, R. B. Robinson, and M.R. Rosen, "I(Kr) contributes to the altered ventricular repolarization that determines long-term cardiac memory," Cardiovasc. Res., vol. 71, pp. 88-96, 2006.
41. M. J. Burgess, L. S. Green, K. Millar, R. Wyatt, and J. A. Abildskov, "The sequence of normal ventricular recovery," Amer. Heart J., vol. 84, pp. 660-669, 1972.
42. C. Patel, J. F. Burke, H. Patel, P. Gupta, P. R. Kowey, C. Antzelevitch, and G. X. Yan, "Is there a significant transmural gradient in repolarization time in the intact heart? cellular basis of the T wave: A century of controversy," Circ. Arrhythm. Electrophysiol., vol. 2, pp. 80-88, 2009.
43. T. Watanabe, P. M. Rautaharju, and T. F. McDonald, "Ventricular action potentials, ventricular extracellular potentials, and the ECG of guinea pig," Circ. Res., vol. 57, pp. 362-373, 1985.
44. S. M. Bryant, X. Wan, S. J. Shipsey, and G. Hart, "Regional differences in the delayed rectifier current (IKr and IKs) contribute to the differences in action potential duration in basal left ventricular myocytes in guinea-pig," Cardiovasc. Res., vol. 40, pp. 322-331, 1998.
45. M. V. Brahmajothi, M. J. Morales, K. A. Reimer, and H. C. Strauss, "Regional localization of ERG, the channel protein responsible for the rapid current of the delayed rectifier, K+ current in the ferret heart," Circ. Res., vol. 81, pp. 128-135, 1997.
46. N. Szentadrassy, T. Banyasz, T. Biro, G. Szabo, B. I. Toth, J. Magyar, J. Lazar, A. Varro, L. Kovacs, and P. P. Nanasi, "Apico-basal inhomogeneity in distribution of ion channels in canine and human ventricular myocardium," Cardiovasc. Res., vol. 65, pp. 851-860, 2005.
47. M. J. Janse, E. A. Sosunov, R. Coronel, T. Opthof, E. P. Anyukhovsky, J. M. T. de Bakker, A. N. Plotnikov, I. N. Shlapakova, P. Danilo, J. G. P. Tijssen, and M. R. Rosen, "Repolarization gradients in the canine left ventricle before and after induction of short-term cardiac memory," Circulation, vol. 112, pp. 1711-1718, 2005.
48. A. Bauer, R. Becker, C. Karle, K. D. Schreiner, J. C. Senges, F. Voss, P. Kraft, W. Kuebler, and W. Schoels, "Effects of the I(Kr)-blocking agent dofetilide and of the {I(Ks)}-blocking agent chromanol 293b on regional disparity of left ventricular repolarization in the intact canine heart," J. Cardiovasc. Pharm., vol. 39, pp. 460-467, 2002.
49. J. Cheng, K. Kamiya, W. Liu, Y. Tsuji, J. Toyama, and I. Kodama, "Heterogeneous distribution of the two components of delayed rectifier K+ current: a potential mechanism of the proarrhythmic effects of methanesulfonanilide class III agents," Cardiovasc Res., vol. 43, pp. 135-147, 1999.
50. T. Watanabe, L. Delbridge, J. O. Bustanmante, and T. F. McDonald, "Heterogeneity of the action potential in isolated rat ventricular myocytes and tissue," Circ. Res., vol. 52, pp. 280-290, 1983.
51. J. M. D. Diego, Z. Q. Sun, and C. Antzelevitch, "Ito and action potential notch are smaller in left versus right canine ventricular epicardium," Amer. J. Physiol., vol. 271, pp. H548-H561, 1996.
52. M. A. Vos, S. H. de Groot, S. C. Verduyn, J. van der Zande, H. D. Leunissen, J. P. Cleutjens, M. van Bilsen, M. J. Daemen, J. J. Schreuder, M. A. Allessie, and H. J. Wellens, "Enhanced susceptibility for acquired torsade de pointes arrhythmias in the dog with chronic, complete AV block is related to cardiac hypertrophy and electrical remodeling," Circulation, vol. 98, pp. 1125-1135, 1998.
53. P. G. Volders, K. R. Sipido, E. Carmeliet, R. L. Spatjens, H. J. Wellens, and M. A. Vos, "Repolarizing K+ currents ITO1 and IKs are larger in right than left canine ventricular midmyocardium," Circulation, vol. 99, pp. 206-210, 1999.
54. F. H. Samie, O. Berenfeld, J. Anumonwo, S. F. Mironov, S. Udassi, J. Beaumont, S. Taffet, A. M. Pertsov, and J. Jalife, "Rectification of the background potassium current: a determinant of rotor dynamics in ventricular fibrillation," Circ. Res., vol. 89, pp. 1216-1223, 2001.
55. G. Seemann, F. B. Sachse, M. Karl, D. L. Weiss, V. Heuveline, and O. Dössel, "Framework for modular, flexible and efficient solving the cardiac bidomain equation using petsc," Prog. Ind. Math., vol. 15, pp. 363-369, 2010.
56. D. W. Liu and C. Antzelevitch, "Characteristics of the delayed rectifier current (IKr and IKs) in canine ventricular epicardial, midmyocardial, and endocardial myocytes. A weaker IKs contributes to the longer action potential of the M cell," Circ. Res., vol. 76, pp. 351-365, 1995.
57. V. S. Chauhan, E. Downar, K. Nanthakumar, J. D. Parker, H. J. Ross, W. Chan, and P. Picton, "Increased ventricular repolarization heterogeneity in patients with ventricular arrhythmia vulnerability and cardiomyopathy: A human in vivo study," Amer. J. Physiol. Heart Circ. Physiol., vol. 290, pp. H79-H86, 2006.
58. S. Yuan, O. Kongstad, E. Hertervig, M. Holm, E. Grins, and B. Olsson, "Global repolarization sequence of the ventricular endocardium: Monophasic action potential mapping in swine and humans," Pacing Clin. Electrophysiol., vol. 24, pp. 1479-1488, 2001.
59. M. R. Franz, K. Bargheer, W. Rafflenbeul, A. Haverich, and P. R. Lichtlen, "Monophasic action potential mapping in human subjects with normal electrocardiograms: Direct evidence for the genesis of the T wave," Circulation, vol. 75, pp. 379-386, 1987.
60. G. Autenrieth, B. Surawicz, and C. S. Kuo, "Sequence of repolarization on the ventricular surface in the dog," Amer. Heart J., vol. 89, pp. 463-469, 1975.
61. J. C. Cowan, C. J. Hilton, C. J. Griffiths, S. Tansuphaswadikul, J. P.Bourke, A. Murray, and R. W. Campbell, "Sequence of epicardial repolarisation and configuration of the T wave," Brit. Heart J., vol. 60, pp. 424-433, 1988.
62. S. Gabriel, R.W. Lau, and C. Gabriel, "The dielectric properties of biological tissues: III. Parametric models for the dielectric spectrum of tissues," Phys. Med. Biol., vol. 41, pp. 2271-2293, 1996.
63. D. U. J. Keller, F. M. Weber, G. Seemann, and O. Dössel, "Ranking the influence of tissue conductivities on forward-calculated ECGs," IEEE Trans. Biomed. Eng., vol. 57, no. 7, pp. 1568-1576, Jul. 2010.
64. A. Khawaja, S. Sanyal, and O. Dössel, "A wavelet-based technique for baseline wander correction in ECG and multi-channel ECG," in Proc. IFMBE, 2005, vol. 9, pp. 291-292.
65. A. Khawaja, Automatic ECG Analysis Using Principal Component Analysis and Wavelet Transformation, vol. 3 (Karlsruhe Transactions on Biomedical Engineering). Karlsruhe, Germany: Universitätsverlag Karlsruhe, 2006.
66. S. T. Morita, D. P. Zipes, H. Morita, and J. Wu, "Analysis of action potentials in the canine ventricular septum: No phenotypic expression of M cells," Cardiovasc. Res., vol. 74, pp. 96-103, 2007.
67. A. Bauer, R. Becker, K. D. Freigang, J. C. Senges, F. Voss, A. Hansen, M. Muller, H. J. Lang, U. Gerlach, A. Busch, P. Kraft, W. Kubler, and W. Schols, "Rate- and site-dependent effects of propafenone, dofetilide, and the new I(Ks)-blocking agent chromanol 293b on individual muscle layers of the intact canine heart," Circulation, vol. 100, pp. 2184-2190, 1999.
68. F.Voss, T. Opthof, J. Marker, A. Bauer, H. A. Katus, and R. Becker, "There is no transmural heterogeneity in an index of action potential duration in the canine left ventricle," Heart Rhythm, vol. 6, pp. 1028-1034, 2009.
69. A. Rodriguez-Sinovas, J. Cinca, A. Tapias, L. Armadans, M. Tresanchez, and J. Soler-Soler, "Lack of evidence of M-cells in porcine left ventricular myocardium," Cardiovasc. Res., vol. 33, pp. 307-313, 1997.
70. W. Kong, N. Fakhari, O. F. Sharifov, R. E. Ideker, W. M. Smith, and V. G. Fast, "Optical measurements of intramural action potentials in isolated porcine hearts using optrodes," Heart Rhythm, vol. 4, pp. 1430-1436, 2007.
71. S. J. Shipsey, S. M. Bryant, and G. Hart, "Effects of hypertrophy on regional action potential characteristics in the rat left ventricle: A cellular basis for T-wave inversion?," Circulation, vol. 96, pp. 2061-2068, 1997.
72. C. E. Conrath and T. Opthof, "Ventricular repolarization: An overview of (patho)physiology, sympathetic effects and genetic aspects," Prog. Biophys. Mol. Biol., vol. 92, pp. 269-307, 2006.
73. T. Opthof, R. Coronel, and M. J. Janse, "Is there a significant transmural gradient in repolarization time in the intact heart?: Repolarization gradients in the intact heart," Circ. Arrhythm. Electrophysiol., vol. 2, pp. 89-96, 2009.
74. P. Taggart, P. M. Sutton, T. Opthof, R. Coronel, R. Trimlett, W. Pugsley, and P. Kallis, "Transmural repolarisation in the left ventricle in humans during normoxia and ischaemia," Cardiovasc. Res., vol. 50, pp. 454-462, 2001.
75. C. Antzelevitch, W. Shimuzu, G. X. Yan, S. Sicouri, J. Weissenburger, V. V. Nesterenko, A. Burashnikov, J. M. D. Diego, J. E. Saffitz, and G. P. Thomas, "The M cell: Its contribution to the ECG and to normal and abnormal electrical function of the heart," J. Cardiovasc. Electr., vol. 10, pp. 1124-1152, 1999.
76. C. Antzelevitch, "Are M cells present in the ventricular myocardium of the pig? A question of maturity," Cardiovasc. Res., vol. 36, pp. 127-128, 1997.
77. S. Poelzing, "Are electrophysiologically distinct M-cells a characteristic of the wedge preparation?," Heart Rhythm, vol. 6, pp. 1035-1037, 2009.
78. R. W. Dos Santos, F. Otaviano Campos, L. Neumann Ciuffo, A. Nygren, W. Giles, and H.Koch, "Atx-ii effects on the apparent location ofmcells in a computationalmodel of a human left ventricular wedge," J. Cardiovasc. Electr., vol. 17, pp. S86-S95, 2006.
79. J. M. Lupoglazoff, I. Denjoy, M. Berthet, N. Neyroud, L. Demay, P. Richard, B. Hainque, G. Vaksmann, D. Klug, A. Leenhardt, G. Maillard, P. Coumel, and P. Guicheney, "Notched T waves on holter recordings enhance detection of patients with LQT2 (herg) mutations," Circulation, vol. 103, pp. 1095-1101, 2001.
80. D. L. Weiss, G. Seemann, D. U. J. Keller, D. Farina, F. B. Sachse, and O. Doessel, "Modeling of heterogeneous electrophysiology in the human heart with respect to ecg genesis," Comput. Cardiol., vol. 34, pp. 49-52, 2007.
81. J. Wu, J. A. Kors, P. R. Rijnbeek, G. van Herpen, Z. Lu, and C. Xu, "Normal limits of the electrocardiogram in chinese subjects," Int. J. Cardiol., vol. 87, pp. 37-51, 2003.
82. N. P. Smith, M. L. Buist, and A. J. Pullan, "Altered t wave dynamics in a contracting cardiac model," J. Cardiovasc. Electr., vol. 14, pp. S203-S209, 2003.
83. M. L. Buist and A. J. Pullan, "The effect of torso impedance on epicardial and body surface potentials: A modeling study," IEEE Trans. Biomed. Eng., vol. 50, no. 7, pp. 816-824, Jul. 2003.
84. M. J. Bishop and G. Plank, "Representing cardiac bidomain bath-loading effects by an augmented monodomain approach: Application to complex ventricular models," IEEE Trans. Biomed. Eng., vol. 58, no. 4, pp. 1066-1075, Apr. 2011.
85. D. A. Hooks, K. A. Tomlinson, S. G. Marsden, I. J. LeGrice, B. H. Smaill, A. J. Pullan, and P. J. Hunter, "Cardiac microstructure: Implications for electrical propagation and defibrillation in the heart," Circ. Res., vol. 91, pp. 331-338, 2002.