Modeling cardiac electromechanics and mechanoelectrical coupling in dyssynchronous and failing hearts: Insight from adaptive computer models

Journal of Cardiovascular Translational Research

Volumn 5, Issue 2, 2012, Pages 159-169

  Kuijpers, Nico H L ^a   Hermeling, Evelien ^a   Bovendeerd, Peter H M ^b   Delhaas, Tammo ^a   Prinzen, Frits W ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Adaptive modeling; Cardiac dyssynchrony; Heart failure; Mechanoelectrical coupling; Multi scale model; Patient specific model

Indexed keywords

CALCIUM;

CALCIUM TRANSPORT; CARDIAC ELECTROMECHANICS; CARDIAC MECHANOELECTRICAL COUPLING; CARDIOVASCULAR PARAMETERS; COMPUTER MODEL; COMPUTER SIMULATION; EXCITATION CONTRACTION COUPLING; FEEDBACK SYSTEM; HEART DYSSYNCHRONY; HEART ELECTROPHYSIOLOGY; HEART FAILURE; HEART HEMODYNAMICS; HEART LEFT BUNDLE BRANCH BLOCK; HEART MUSCLE CONDUCTION DISTURBANCE; HEART MUSCLE POTENTIAL; HEART PACING; HUMAN; ION CURRENT; MATHEMATICAL MODEL; MECHANICAL STRESS; NONHUMAN; PRIORITY JOURNAL; PULMONARY HYPERTENSION; REVIEW; STRESS STRAIN RELATIONSHIP;

ACTION POTENTIALS; BIOMECHANICS; COMPUTER SIMULATION; HEART FAILURE; HEART VENTRICLES; HUMANS; MODELS, CARDIOVASCULAR; MODELS, THEORETICAL; MYOCARDIAL CONTRACTION;

EID: 84866129399     PISSN: 19375387     EISSN: 19375395     Source Type: Journal    
DOI: 10.1007/s12265-012-9346-y     Document Type: Review

References (97)

1. Aguado-Sierra, J., Krishnamurthy,A., Villongco, C., Chuang, J., Howard, E., Gonzales, M. J., et al. (2011). Patient-specific modeling of dyssynchronous heart failure: A case study. Progress in Biophysics and Molecular Biology, 107, 147-155.
2. Aiba, T., Hesketh, G. G., Barth, A. S., Liu, T., Daya, S., Chakir, K., et al. (2009). Electrophysiological consequences of dyssynchronous heart failure and its restoration by resynchronization therapy. Circulation, 119, 1220-1230.
3. Arts, T., Bovendeerd, P., Delhaas, T., & Prinzen, F. (2003). Modeling the relation between cardiac pump function and myofiber mechanics. Journal of Biomechanics, 36, 731-736. (Pubitemid 36407625)
4. Arts, T., Bovendeerd, P. H. M., Prinzen, F. W., & Reneman, R. S. (1991). Relation between left ventricular cavity pressure and volume and systolic fiber stress and strain in the wall. Biophysical Journal, 59, 93-102.
5. Arts, T., Delhaas, T., Bovendeerd, P., Verbeek, X., & Prinzen, F. W. (2005). Adaptation to mechanical load determines shape and properties of heart and circulation: The Circ-Adapt model. American Journal of Physiology. Heart and Circulatory Physiology, 288, H1943-H1954. (Pubitemid 40418025)
6. Arts, T., Prinzen, F. W., Snoeckx, L. H., Rijcken, J. M., & Reneman, R. S. (1994). Adaptation of cardiac structure by mechanical feedback in the environment of the cell: A model study. Biophysical Journal, 66, 953-961. (Pubitemid 24106341)
7. Arts, T., Reneman, R. S., & Veenstra, P. C. (1979). A model of the mechanics of the left ventricle. Annals of Biomedical Engineering, 7, 299-318. (Pubitemid 10109942)
8. Bers, D. M. (2002). Cardiac excitation-contraction coupling. Nature, 415, 198-205. (Pubitemid 34059525)
9. Bovendeerd, P. H. M., Arts, T., Huyghe, J. M., van Campen, D. H., & Reneman, R. S. (1994). Influence of endocardial-epicardial crossover of muscle fibers on left ventricular wall mechanics. Journal of Biomechanics, 27, 941-951. (Pubitemid 24169717)
10. Bovendeerd, P. H. M., Arts, T., Huyghe, J. M., van Campen, D. H., & Reneman, R. S. (1996). Regional wall mechanics in the ischemic left ventricle: Numerical modeling and dog experiments. The American Journal of Physiology, 270, H398-H410.
11. Campbell, S. G., Lionetti, F. V., Campbell, K. S., & McCulloch, A. D. (2010). Coupling of adjacent tropomyosins enhances cross-bridge-mediated cooperative activation in a Markov model of the cardiac thin filament. Biophysical Journal, 98, 2254-2264.
12. Colli-Franzone, P., Guerri, L., & Tentoni, S. (1990). Mathematical modeling of the excitation process in myocardial tissue: Influence of fiber rotation on wavefront propagation and potential field. Mathematical Biosciences, 101, 155-235. (Pubitemid 20357966)
13. Courtemanche, M., Ramirez, R. J., & Nattel, S. (1998). Ionic mechanisms underlying human atrial action potential properties: Insights from a mathematical model. American Journal of Physiology. Heart and Circulatory Physiology, 275, H301-H321.
14. Grandi, E., Pandit, S. V., Voigt, N., Workman, A. J., Dobrev, D., Jalife, J., et al. (2011). Human atrial action potential and Ca2+ model. Circulation Research, 109, 1055-1066.
15. Grandi, E., Pasqualini, F. S., & Bers, D. M. (2010). A novel computational model of the human ventricular action potential and Ca transient. Journal of Molecular and Cellular Cardiology, 48, 112-121.
16. Greenstein, J. L., & Winslow, R. L. (2011). Integrative systems models of cardiac excitation-contraction coupling. Circulation Research, 108, 70-84.
17. Gurev, V., Constantino, J., Rice, J. J., & Trayanova, N. A. (2010). Distribution of electromechanical delay in the heart: Insights from a three-dimensional electromechanical model. Biophysical Journal, 99, 745-754.
18. Henriquez, C. S. (1993). Simulating the electrical behavior of cardiac tissue using the bidomain model. Critical Reviews in Biomedical Engineering, 21, 1-77. (Pubitemid 23106742)
19. Hermeling, E., Verhagen, T. M., Prinzen, F. W., & Kuijpers, N. H. L. (2009). Transmural heterogeneity in ion channel properties in the left ventricle optimizes pump function during natural electrical activation. Computers in Cardiology, 36, 397-400.
20. Hill, A. V. (1938). The heat of shortening and the dynamic constants in muscle. Proceedings of the Royal Society of London, 126, 136-195.
21. Hodgkin, A. L., & Huxley, A. F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology, 117, 500-544.
22. Humphrey, J. D., & Rajagopal, K. R. (2002). A constrained mixture model for growth and remodeling of soft tissues. Mathematical Models and Methods in Applied Sciences, 12, 407-430.
23. Huxley, A. F. (1957). Muscle structure and theories of contraction. Progress in Biophysics and Biophysical Chemistry, 7, 255-318.
24. Iyer, V., Mazhari, R., & Winslow, R. L. (2004). A computational model of the human left-ventricular epicardial myocyte. Biophysical Journal, 87, 1507-1525. (Pubitemid 39167010)
25. Jeyaraj, D., Wilson, L. D., Zhong, J., Flask, C., Saffitz, J. E., Deschênes, I., et al. (2007). Mechanoelectric feedback as novel mechanism of cardiac electrical remodeling. Circulation, 115, 3145-3155. (Pubitemid 47012229)
26. Jie, X., Gurev, V., & Trayanova, N. (2010). Mechanisms of mechanically induced spontaneous arrhythmias in acute regional ischemia. Circulation Research, 106, 185-192.
27. Kääb, S., Nuss, B., Chiamvimonvat, N., O'Rourke, B., Pak, P. H., Kass, D. A., et al. (1996). Ionic mechanisms of action potential prolongation in ventricular myocytes from dogs with pacing-induced heart failure. Circulation Research, 78, 262-273. (Pubitemid 26040856)
28. Keener, J. P., & Sneyd, J. (1998). Mathematical physiology. New York: Springer.
29. Keldermann, R. H., Nash, M. P., Gelderblom, H., Wang, V. Y., & Panfilov, A. V. (2010). Electromechanical wavebreak in a model of the human left ventricle. American Journal of Physiology. Heart and Circulatory Physiology, 299, H134-H143.
30. Keldermann, R. H., Ten Tusscher, K. H. W. J., Nash, M. P., Bradley, C. P., Hren, R., Taggart, P., et al. (2009). A computational study of mother rotor VF in the human ventricles. American Journal of Physiology. Heart and Circulatory Physiology, 296, H370-H379.
31. Kerckhoffs, R. C. P., Faris, O. P., Bovendeerd, P. H. M., Prinzen, F. W., Smits, K., McVeigh, E. R., et al. (2003). Timing of depolarization and contraction in the paced canine left ventricle: Model and experiment. Journal of Cardiovascular Electrophysiology, 14, S188-S195. (Pubitemid 37393002)
32. Kerckhoffs, R. C. P., Faris, O. P., Bovendeerd, P. H. M., Prinzen, F. W., Smits, K., McVeigh, E. R., et al. (2005). Electromechanics of paced left ventricle simulated by straightforward mathematical model: Comparison with experiments. American Journal of Physiology. Heart and Circulatory Physiology, 289, H1889-H1897. (Pubitemid 41507337)
33. Kerckhoffs, R. C. P., Healy, S. N., Usyk, T. P., & McCulloch, A. D. (2006). Computational methods for cardiac electromechanics. Proceedings of the IEEE, 94, 769-783.
34. Kerckhoffs, R. C. P., Lumens, J., Vernooy, K., Omens, J. H., Mulligan, L. J., Delhaas, T., et al. (2008). Cardiac resynchronization: Insight from experimental and computational models. Progress in Biophysics and Molecular Biology, 97, 543-561.
35. Kerckhoffs, R. C. P., McCulloch, A. D., Omens, J. H., & Mulligan, L. J. (2009). Effects of biventricular pacing and scar size in a computational model of the failing heart with left bundle branch block. Medical Image Analysis, 13, 362-369.
36. Kerckhoffs, R. C. P., Omens, J. H., McCulloch, A. D., & Mulligan, L. J. (2010). Ventricular dilation and electrical dyssynchrony synergistically increase regional mechanical nonuniformity but not mechanical dyssynchrony: A computational model. Circulation: Heart Failure, 3, 528-536.
37. Kohl, P., & Sachs, F. (2001). Mechanoelectric feedback in cardiac cells. Philosophical Transactions of the Royal Society of London, 359, 1173-1185.
38. Kooshkabadi, M., Whalen, P., Yoo, D., & Langberg, J. (2009). Stretch-activated receptors mediate cardiac memory. PACE, 32, 330-335.
39. Kroon, W., Delhaas, T., Arts, T., & Bovendeerd, P. H. M. (2009). Computational modeling of volumetric soft tissue growth: Application to the cardiac left ventricle. Biomechanics and Modeling in Mechanobiology, 8, 301-309.
40. Kroon, W., Delhaas, T., Bovendeerd, P. H. M., & Arts, T. (2009). Computational analysis of the myocardial structure: Adaptation of cardiac myofiber orientations through deformation. Medical Image Analysis, 13, 346-353.
41. Kuijpers, N. H. L., Ten Eikelder, H. M. M., Bovendeerd, P. H. M., Verheule, S., Arts, T., & Hilbers, P. A. J. (2007). Mechanoelectric feedback leads to conduction slowing and block in acutely dilated atria: A modeling study of cardiac electromechanics. American Journal of Physiology. Heart and Circulatory Physiology, 292, H2832-H2853. (Pubitemid 47084533)
42. Kuijpers, N. H. L., Ten Eikelder, H. M. M., Bovendeerd, P. H. M., Verheule, S., Arts, T., & Hilbers, P. A. J. (2008). Mechanoelectrical feedback as a trigger mechanism for cardiac electrical remodeling:Amodel study. Annals of Biomedical Engineering, 36, 1816-1835.
43. Kuijpers, N. H. L., Hermeling, E., & Prinzen, F. W. (2010). Mechano-electrical feedback during cardiac resynchronization therapy? Computers in Cardiology, 37, 833-836.
44. Kuijpers, N. H. L., Potse, M., Van Dam, P. M., Ten Eikelder, H. M. M., Verheule, S., Prinzen, F. W., et al. (2011). Mechanoelectrical coupling enhances initiation and affects perpetuation of atrial fibrillation during acute atrial dilation. Heart Rhythm, 8, 429-436.
45. LeGrice, I. J., Smaill, B. H., Chai, L. Z., Edgar, S. G., Gavin, J. B., & Hunter, P. J. (1995). Laminar structure of the heart: Ventricular myocyte arrangement and connective tissue architecture in the dog. The American Journal of Physiology, 269, H571-H582.
46. Lin, I. E., & Taber, L. A. (1995). A model for stress-induced growth in the developing heart. Journal of Biomechanical Engineering, 117, 343-349.
47. Lumens, J., Arts, T., Broers, B., Boomars, K. A., Van Paassen, P., Prinzen, F. W., et al. (2009). Right ventricular free wall pacing improves cardiac pump function in severe pulmonary arterial hypertension: A computer simulation analysis. American Journal of Physiology. Heart and Circulatory Physiology, 297, H2196-H2205.
48. Lumens, J., Blanchard, D. G., Arts, T., Mahmud, E., & Delhaas, T. (2010). Left ventricular underfilling and not septal bulging dominates abnormal left ventricular filling hemodynamics in chronic thromboembolic pulmonary hypertension. American Journal of Physiology. Heart and Circulatory Physiology, 299, H1083-H1091.
49. Lumens, J., Delhaas, T., Kirn, B., & Arts, T. (2009). Threewall segment (TriSeg) model describing mechanics and hemodynamics of ventricular interaction. Annals of Biomedical Engineering, 37, 2234-2255.
50. Luo, C. H., & Rudy, Y. (1994). A dynamic model of the cardiac ventricular action potential. I. Simulations of ionic currents and concentration changes. Circulation Research, 74, 1071-1096. (Pubitemid 24176903)
51. Medina-Ravell, V. A., Lankipalli, R. S., Yan, G. X., Antzelevitch, C., Medina-Malpica, N. A., Medina-Malpica, O. A., et al. (2003). Effect of epicardial or biventricular pacing to prolong QT interval and increase transmural dispersion of repolarization. Circulation, 107, 740-746.
52. Nash, M. P., & Hunter, P. J. (2000). Computational mechanics of the heart. Journal of Elasticity, 61, 131-141.
53. Nickerson, D., Smith, N., & Hunter, P. (2005). New developments in a strongly coupled cardiac electromechanical model. Europace, 7, S118-S127. (Pubitemid 41244894)
54. Niederer, S. A., Hunter, P. J., & Smith, N. P. (2006). A quantitative analysis of cardiac myocyte relaxation: A simulation study. Biophysical Journal, 90, 1697-1722.
55. Niederer, S. A., Plank, G., Chinchapatnam, P., Ginks, M., Lamata, P., Rhode, K. S., et al. (2011). Length-dependent tension in the failing heart and the efficacy of cardiac resynchronization therapy. Cardiovascular Research, 89, 336-343.
56. Niederer, S. A., Shetty, A. K., Plank, G., Bostock, J., Razavi, R., Smith, N. P., et al. (2011). Biophysical modeling to simulate the response to multisite left ventricular stimulation using a quadripolar pacing lead. PACE. doi:10.1111/j.1540-8159.2011.03243.x.
57. Niederer, S. A., & Smith, N. P. (2009). The role of the Frank-Starling law in the transduction of cellular work to whole organ pump function: A computational modeling analysis. PLoS Computational Biology, 5, e1000371.
58. Niederer, S. A., Ter Keurs, H. E., & Smith, N. P. (2009). Modelling and measuring electromechanical coupling in the rat heart. Experimental Physiology, 94, 529-540.
59. Nordsletten, D. A., Niederer, S. A., Nash, M. P., Hunter, P. J., & Smith, N. P. (2011). Coupling multi-physics models to cardiac mechanics. Progress in Biophysics and Molecular Biology, 104, 77-88.
60. Nygren, A., Fiset, C., Firek, L., Clark, J. W., Lindblad, D. S., &Clark,R. B. (1998).Mathematicalmodel of an adult human atrial cell; the role of K+ currents in repolarization. Circulation Research, 82, 63-81. (Pubitemid 28074020)
61. O'Hara, T., Virág, L., Varró, A., & Rudy, Y. (2011). Simulation of the undiseased human cardiac ventricular action potential: Model formulation and experimental validation. PLoS Computational Biology, 7, e1002061.
62. Omens, J. H., & Fung, Y. C. (1990). Residual strain in rat left ventricle. Circulation Research, 66, 37-45. (Pubitemid 20033924)
63. O'Rourke, B., Kass, D. A., Tomaselli, G. F., Kääb, S., Tunin, R., & Marbán, E. (1999). Mechanisms of altered excitation-contraction coupling in canine tachycardia-induced heart failure, I: experimental studies. Circulation Research, 84, 562-570. (Pubitemid 29138593)
64. Piacentino III, V., Weber, C. R., Chen, X., Weisser-Thomas, J., Margulies, K. B., Bers, D. M., et al. (2003). Cellular basis of abnormal calcium transients of failing human ventricular myocytes. Circulation Research, 92, 651-658. (Pubitemid 36417700)
65. Plotnikov, A. N., Yu, H., Geller, J. C., Gainullin, R. Z., Chandra, P., Patberg, K. W., et al. (2003). Role of L-type calcium channels in pacing-induced short-term and longterm cardiac memory in canine heart. Circulation, 107, 2844-2849. (Pubitemid 36705996)
66. Potse, M. (2012). Mathematical modeling and simulation of ventricular activation sequence: implications for CRT. Journal of Cardiovascular Translational Research. doi:10.1007/s12265-011-9343-6.
67. Potse, M., Dubé, B., Richer, J., Vinet, A., & Gulrajani, R. M. (2006). A comparison of monodomain and bidomain reaction-diffusion models for action potential propagation in the human heart. IEEE Transactions on Biomedical Engineering, 53, 2425-2435. (Pubitemid 46019529)
68. Priebe, L., & Beuckelmann, D. J. (1998). Simulation study of cellular electric properties in heart failure. Circulation Research, 82, 1206-1223. (Pubitemid 28311128)
69. Prinzen, F. W., Augustijn, C. H., Arts, T., Allessie, M. A., & Reneman, R. S. (1990). Redistribution of myocardial fiber strain and blood flow by asynchronous activation. The American Journal of Physiology, 259, H300-H308. (Pubitemid 20259403)
70. Prinzen, F. W., Hunter, W. C., Wyman, B. T., & McVeigh, E. R. (1999).Mapping of regional myocardial strain and work during ventricular pacing: Experimental study usingmagnetic resonance imaging tagging. Journal of the American College of Cardiology, 33, 1735-1742.
71. Prinzen, F. W., Vernooy, K., De Boeck, B. W., & Delhaas, T. (2011). Mechano-energetics of the asynchronous and resynchronized heart. Heart Failure Reviews, 16, 215-224.
72. Rademakers, L. M., De Boeck, B. W., Maessen, J. G., & Prinzen, F. W. (2008). Development of strategies for guiding cardiac resynchronization therapy. Heart Failure Clinics, 4, 333-345. (Pubitemid 351885508)
73. Rausch, M., Dam, A., Göktepe, S., Abilez, O. J., & Kuhl, E. (2010). Computationalmodeling of growth: Systemic and pulmonary hypertension in the heart. Biomechanics and Modeling in Mechanobiology, 10:799-811.
74. Rice, J. J., & De Tombe, P. P. (2008). Approaches to modeling crossbridges and calcium-dependent activation in cardiac muscle. Progress in Biophysics and Molecular Biology, 85, 179-195.
75. Rice, J. J., Wang, F., Bers, D. M., & De Tombe, P. P. (2008). Approximate model of cooperative activation and crossbridge cycling in cardiac muscle using ordinary differential equations. Biophysical Journal, 95, 2368-2390.
76. Rice, J. J., Winslow, R. L., & Hunter, W. C. (1999). Comparison of putative cooperative mechanisms in cardiac muscle: Length dependence and dynamic responses. American Journal of Physiology. Heart and Circulatory Physiology, 276, H1734-H1754. (Pubitemid 29246563)
77. Rodriguez, E. K., Hoger, A., & McCulloch, A. D. (1994). Stress-dependent finite growth in soft elastic tissues. Journal of Biomechanics, 27, 455-467. (Pubitemid 24102058)
78. Rosenbaum, M. B., Blanco, H. H., Elizari, M. V., Lazzari, J. O., & Davidenko, J. M. (1982). Electrotonic modulation of the T wave and cardiac memory. The American Journal of Cardiology, 50, 213-222. (Pubitemid 12059013)
79. Skalak, R., Dasgupta, G., Moss, M., Otten, E., Dullumeijer, P., & Vilmann, H. (1982). Analytical description of growth. Journal of Theoretical Biology, 94, 555-577. (Pubitemid 12154339)
80. Sosunov, E. A., Anyukhovsky, E. P., & Rosen, M. R. (2008). Altered ventricular stretch contributes to initiation of cardiac memory. Heart Rhythm 5, 106-113.
81. Taber, L. A., & Chabert, S. (2002). Theoretical and experimental study of growth and remodeling in the developing heart. Biomechanics and Modeling in Mechanobiology, 1, 29-43.
82. Taber, L. A., & Perucchio, R. (2000). Modeling heart development. Journal of Elasticity, 61, 165-197. (Pubitemid 32723828)
83. Trayanova, N., Plank, G., & Rodríguez, B. (2006).What have we learned from mathematical models of defibrillation and postshock arrhythmogenesis? application of bidomain simulations. Heart Rhythm, 3, 1232-1235. (Pubitemid 44464140)
84. Trayanova, N. A. (2011). Whole-heart modeling: Applications to cardiac electrophysiology and electromechanics. Circulation Research, 108, 113-128.
85. Trayanova, N. A., & Rice, J. J. (2011). Cardiac electromechanical models: From cell to organ. Frontiers in Physiology, 2, 43.
86. Tung, L. (1978). A bi-domain model for describing ischemic myocardial D-C potentials. Ph.D. thesis, MIT, Cambridge, Massachusetts, USA.
87. Ten Tusscher, K. H. W. J., Hren, R., & Panfilov, A. V. (2007). Organization of ventricular fibrillation in the human heart. Circulation Research, 100, 87-101.
88. Ten Tusscher, K. H. W. J., Noble, D., Noble, P. J., & Panfilov, A. V. (2004).Amodel for human ventricular tissue. American Journal of Physiology. Heart and Circulatory Physiology, 286, H1573-H1589.
89. Ten Tusscher, K. H. W. J., & Panfilov, A. V. (2006). Alternans and spiral breakup in a human ventricular tissue model. American Journal of Physiology. Heart and Circulatory Physiology, 291, H1088-H1100. (Pubitemid 44343652)
90. Usyk, T. P., & McCulloch, A. D. (2003). Electromechanical model of cardiac resynchronization in the dilated failing heart with left bundle branch block. Journal of Electrocardiology, 36, 57-61. (Pubitemid 38049762)
91. Usyk, T. P., & McCulloch, A. D. (2003). Relationship between regional shortening and asynchronous electrical activation in a three-dimensional model of ventricular electromechanics. Journal of Cardiovascular Electrophysiology, 14, S196-S202. (Pubitemid 37393003)
92. Van Geldorp, I. E., Vernooy, K., Delhaas, T., Prins, M. H., Crijns, H. J., Prinzen, F. W., et al. (2010). Beneficial effects of biventricular pacing in chronically right ventricular paced patients with mild cardiomyopathy. Europace, 12, 223-229.
93. Vernooy, K., Cornelussen, R. N. M., Verbeek, X. A. A. M., Vanagt, W. Y. R., van Hunnik, A., Kuiper, M., et al. (2007). Cardiac resynchronization therapy cures dyssynchronopathy in canine left bundle-branch block hearts. European Heart Journal, 28, 2148-2155. (Pubitemid 47517434)
94. Vernooy, K., Verbeek, X. A. A. M., Peschar, M., Crijns, H. J. G. M., Arts, T., Cornelussen, R. N. M., et al. (2005). Left bundle branch block induces ventricular remodelling and functional septal hypoperfusion. European Heart Journal, 26, 91-98. (Pubitemid 40221129)
95. Wecke, L., Van Deursen, C. J. M., Bergfeldt, L., & Prinzen, F. W. (2011). Repolarization changes in patients with heart failure receiving cardiac resynchronization therapy -signs of cardiac memory. Journal of Electrocardiology, 44, 590-598.
96. Weiss, J. N., Garfinkel, A., Karagueuzian, H. S., Chen, P. S., & Qu, Z. (2010). Early afterdepolarizations and cardiac arrhythmias. Heart Rhythm, 7, 1891-1899.
97. Winslow, R. L., Rice, J. J., Jafri, M. S., Marbán, E., & O'Rourke, B. (1999). Mechanisms of altered excitation-contraction coupling in canine tachycardia-induced heart failure, II: model studies. Circulation Research, 84, 571-586. (Pubitemid 29138594)