Scroll-wave dynamics in human cardiac tissue: Lessons from a mathematical model with inhomogeneities and fiber architecture

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Majumder, Rupamanjari ^a   Nayak, Alok Ranjan ^a   Pandit, Rahul ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; HEART MUSCLE; HEART MUSCLE CELL; MATHEMATICAL MODEL; MYOFILAMENT; QUALITATIVE ANALYSIS; BIOLOGICAL MODEL; ELECTROPHYSIOLOGY; HEART; HUMAN; METABOLISM; PHYSIOLOGY; ROTATION; TIME;

ELECTROPHYSIOLOGICAL PROCESSES; HEART; HUMANS; MODELS, CARDIOVASCULAR; MYOCARDIUM; ROTATION; TIME FACTORS;

EID: 79953693276     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018052     Document Type: Article

References (70)

1. Clayton RH, Bernus O, Cherry EM, Dierckx H, Fenton FH, et al. (2011) Models of cardiac tissue electrophysiology: Progress, challenges and open questions. Prog Biophys Mol Biol 104: 22-48.
2. Shajahan TK, Sinha S, Pandit R, (2007) Spiral-wave Dynamics Depends Sensitively on Inhomogeneities in Mathematical Models of Ventricular Tissue. Phys. Rev. E 75 011929-1- 011929-8.
3. Shajahan TK, Nayak AR, Pandit R, (2009) Spiral-Wave Turbulence and its Control in the Presence of Inhomogeneities in Four Mathematical Models of Cardiac Tissue. PLoS ONE 4 (3): e4738.
4. Jalife J, Gray RA, Morley GE, Davidenko JM, (1998) Self-organization and the dynamical nature of ventricular fibrillation. Chaos 8 (1): 79-93.
5. Mann DL, (2002) Inflammatory Mediators and the Failing Heart: Past, Present, and the Foreseeable Future. Circ. Res 91: 988-998.
6. Kléber AG, Rudy Y, (2004) Basic Mechanisms of Cardiac Impulse Propagation and Associated Arrhythmias. Physiol. Rev. 84 431-488.
7. Vigmond EJ, Weber dos Santos R, Prassl AJ, Deo M, Plank G, (2008) Solvers for the cardiac bi-domain equations. Progress in Biophysics and Molecular Biology 96: 3-18.
8. Kim YH, Xie F, Yashima M, Wu T-J, Valderrábano M, et al. (1999) Role of Papillary Muscle in the Generation and Maintenance of Reentry During Ventricular Tachycardia and Fibrillation in Isolated Swine Right Ventricle. Circulation 100: 1450-1459.
9. Bub G, Glass L, Publicover NG, Shrier A, (1998) Bursting calcium rotors in cultured cardiac myocyte monolayers. Proc. Natl. Acad. Sci. USA95: 10283-10287.
10. Bub G, Shrier A, Glass L, (2002) Spiral Wave Generation in Heterogeneous Excitable Media. Phys. Rev. Lett 88: 058101.
11. Massé S, Donwar E, Chauhan V, Sevaptisidis E, Nanthakumar K, (2007) Ventricular fibrillation in myopathic human hearts: mechanistic insights from in vivo global endocardial and epicardial mapping. Am. J Physiol. Heart. Circ. Physiol 292: H2589-H2597.
12. Iravanian S, Nabutovsky Y, Kong C-R, Saha S, Bursac N, et al. (2003) Functional reentry in cultured monolayers of neonatal rat cardiac cells. Am. J. Physiol 285: H449-H456.
13. Hwang S, Yea K, Lee KJ, (2004) Regular and Alternant Spiral Waves of Contractile Motion on Rat Ventricle Cell Cultures. Phys. Rev. Lett 92: 198103.
14. Davidenko JM, Kent PF, Chialvo DR, Michaels DC, Jalife J, (1990) Sustained vortex-like waves in normal isolated ventricular muscle. Proc. Natl. Acad. Sci. USA87: 87858789.
15. Witkowski FX, Leon LJ, Penkoske PA, Giles WR, Spano ML, et al. (1998) Spatiotemporal evolution of ventricular fibrillation. Nature 392: 7882.
16. Qu Z, Xie F, Garfinkel A, Weiss JN, (2000) Origins of Spiral Wave Meander and Breakup in a Two-Dimensional Cardiac Tissue Model. Annals of Biomedical Engineering 28: 755771.
17. Hwang S, Kim TY, Lee KJ, (2005) Complex-periodic spiral waves in confluent cardiac cell cultures induced by localized inhomogeneities. Proc. Natl. Acad. Sci. USA102: 10363-10368.
18. Roth BJ, (2001) Meandering of spiral waves in anisotropic cardiac tissue. Physica D 150: 127136.
19. Kuijpers NHL, Keldermann RH, Arts T, Hilbers PAJ, (2005) Computer simulations of successful defibrillation in decoupled and non-uniform cardiac tissue. Europace 7: S166-S177.
20. Cherry EM, Fenton FH, (2008) Visualization of spiral and scroll waves in simulated and experimental cardiac tissue. New Journal of Physics 10: 12501.
21. Rusakov A, Medvinsky AB, Panfilov AV, (2005) Scroll waves meandering in a model of an excitable medium. Phys. Rev.E 72: 022902.
22. Fenton F, Cherry E, Hastings HM, Evans SJ, (2002) Multiple mechanisms of spiral wave break-up in a model of cardiac electrical activity. Chaos 12 (3): 852-892.
23. Ten Tusscher KHWJ, Bernus O, Hren R, Panfilov AV, (2006) Comparison of electro-physiological models for human ventricular cells and tissues. Progress in Biophysics and Molecular Biology 90: 326345.
24. Bueno-Orovio A, Cherry EM, Fenton F, (2008) Minimal model for human ventricular action potentials in tissue. Journal of Theoretical Biology 253: 544-560.
25. Ikeda T, Yashima M, Uchida T, Hough D, Fishbein MC, et al. (1997) Attachment of meandering reentrant wavefronts to anatomic obstacles in the atrium. Circ Res 81: 753.
26. Valderrábano M, Kim YH, Yashima M, Wu TJ, Karagueuzian HS, et al. (2000) Obstacle-induced transition from ventricular fibrillation to tachycardia in isolated swine right ventricles. J Am Coll Cardiol 36.
27. Lim ZY, Maskara B, Aguel F, Emokpae R Jr, Tung L, (2006) Spiral Wave Attachment to Millimeter-Sized Obstacles. Circulation 114: 21132121.
28. Davidenko JM, Pertsov AV, Salomonsz R, Baxter W & Jalife J, (1992) Stationary and drifting spiral waves of excitation in isolated cardiac muscle. Nature 355: 349.
29. Xie F, Qu Z, Garfinkel A, (1998) Dynamics of reentry around a circular obstacle in cardiac tissue. Phys Rev E 58: 6355.
30. Ten Tusscher KHWJ, Panfilov A, (2003) Influence of nonexcitable cells on spiral break-up in two-dimensional and three-dimensional excitable media. Phys Rev E 68: 062902.
31. Starobin JM, Starmer CF, (1996) Boundary-layer analysis of waves propagating in an excitable medium: Medium conditions for wave-front-obstacle separation. Phys Rev E 54: 430.
32. Fenton F & Karma A, (1998) Vortex dynamics in three-dimensional continuous myocardium with fiber rotation: Filament instability and fibrillation. Chaos 8 (1): 20-47.
33. Clayton RH, Panfilov AV, (2008) A guide to modeling cardiac electrical activity in anatomically detailed ventricles. Progress in Biophysics and Molecular Biology 96: 19-43.
34. Gullberg GT, Defrise M, Panin VY, Zeng GL, (2001) Efficient cardiac diffusion tensor MRI by three-dimensional reconstruction of solenoidal tensor fields. Magnetic Resonance Imaging 19: 233-256.
35. Benson AP, Ries ME, Holden AV, (2007) Effects of Geometry and Architecture on Re-entrant Scroll Wave Dynamics in Human Virtual Ventricular Tissues.F.B. Sachse and G. Seemann (Eds.) pp. 200-209 FIMH 2007 LNCS 4466.
36. Qu Z, Kil J, Xie F, Garfinkel A & Weiss JN, (2000) Scroll Wave Dynamics in a Three-Dimensional Cardiac Tissue Model: Roles of Restitution, Thickness, and Fiber Rotation. Biophysical Journal 78: 2761-2775.
37. Fenton FH, Cherry EM, Hastings HM, Evans SJ, (2002) Multiple mechanisms of spiral wave break-up in a model of cardiac electrical activity. Chaos 12: 852-92.
38. Fenton FH, Karma A, (1998) Fiber-rotation-induced vortex turbulence in thick myocardium. Phys. Rev. Lett 81: 481-4.
39. Rappel WJ, (2001) Filament instability and rotational tissue anisotropy: a numerical study using detailed cardiac models. Chaos 11: 71-80.
40. Vigmond EJ, Leon LJ, (2001) Effect of fibre rotation on the initiation of re-entry in cardiac tissue. Med. Biol. Eng. Comput 39: 455-464.
41. Li G, Feng J, Yue L, Carrier M, (1998) Transmural heterogeneity of action potentials and Ito1 in myocytes isolated from the human right ventricle. Am J Physiol Heart Circ Physiol 275: 369-377.
42. Zhang H, Hancox JC, (2004) In silico study of action potential and QT interval shortening due to loss of inactivation of the cardiac rapid delayed rectifier potassium current. Biochemical and Biophysical Research Communications 322: 693-699.
43. Zhang H, Kharche S, Holden AV, Hancox JC, (2008) Repolarisation and vulnerability to re-entry in the human heart with short QT syndrome arising from KCNQ1 mutation-A simulation study. Progress in Biophysics and Molecular Biology 96: 12-131.
44. Ten Tusscher KHWJ, Noble D, Noble PJ, Panfilov AV, (2004) A model for human ventricular tissue. Am. J Physiol. Heart Circ. Physiol pp. 286.
45. Pertsov AM, Davidenko JM, Salomonsz R, Baxter WT, Jalife J, (1993) Spiral Waves of Excitation Underlie Reentrant Activity in Isolated Cardiac Muscle. Circulation Research 72: 3, March.
46. Brugada J, Boersma L, Kirchhof CJ, Heynen VV, Allessie MA, (1991) Reentrant excitation around a fixed obstacle in uniform anisotropic ventricular myocardium. Circulation 84: 1296-1306.
47. Chen JX, et al. (2008) Motion of spiral waves induced by local pacing. Cent.Eur. J Phys 6 (3): 427-433.
48. Panfilov AV, Keldermann RH, Nash MP, (2007) Drift and break-up of spiral waves in reaction-diffusion-mechanics systems. Procs. Nat. Acd. Sci 104: 19 May.
49. Gray RA, Jalife J, Panfilov AV, Baxter WT, Cabo C, et al. (1995) Mechanisms of Cardiac Fibrillation. Science 270 (5239): 1222-3.
50. Pumir A, Sinha S, Sridhar S, Argentina M, Hörning M, et al. (2010) Wave-train-induced termination of weakly anchored vortices in excitable media. Phys Rev E 81 010901.
51. Remy-Jardin M, Remy J, (2008) Integrated Cardiothoracic Imaging with MDCT, (Springer),.
52. Sinha S, Sridhar S, (2008) Controlling spatiotemporal chaos in excitable media using an array of control points. EPL 81: 50002.
53. Sinha S, Stein KM, Christini DJ, (2002) Critical role of inhomogeneities in pacing termination of cardiac reentry. Chaos 12 (3): 893-902.
54. Panfilov A, (1998) Spiral break-up as a model of ventricular fibrillation. Chaos 8 (1): 57-64.
55. Efimov IR, Nikolski VP, Salama G, (2004) Optical Imaging of the Heart. Circ. Res pp. July 21-33.
56. Peters NS, (1996) New insights into myocardial arrhythmogenesis: distribution of gap-junctional coupling in normal, ischaemic and hypertrophied human hearts: Glaxo/MRS young investigator prize. Clin Sci 90: 447-452.
57. Gillis AM, Fast GV, Rohr S, Kléber AG, (2000) Mechanism of Ventricular Defibrillation: The Role of Tissue Geometry in the Changes in Transmembrane Potential in Patterned Myocyte Cultures. Circulation 101: 2438-2445.
58. Dillon SM, Allessie MA, Ursell PC, Wit AL, (1988) Influences of anisotropic tissue structure on reentrant circuits in the epicardial border zone of subacute canine infarcts. Circ. Res 63: 182-206.
59. Winslow, Scollan DF, Holmes A, Yung CK, Zhang J, et al. (2000) Electrophysiological Modeling of Cardiac Ventricular Function: From Cell to Organ. Annu Rev Biomed Eng 2: 119155.
60. Bursac N, Aguel F, Tung L, (2004) Multiarm spirals in a two-dimensional cardiac substrate. Proc. Natl. Acad. Sci. USA101: 15530-15534.
61. Sinha S, Pande A, Pandit R, (2001) Defibrillation via the elimination of spiral turbulence in model for ventricular fibrillation. Phys Rev Lett 86: 3678.
62. Zhang H, Hu B, Hu G, (2003) Suppression of spiral waves and spatiotemporal chaos by generating target waves in excitable media. Phys Rev E 68: 026134.
63. Potse M, Dube B, Richer J, Vinet A, Gulrajani RM, (2006) A comparison of mono-domain and bi-domain reaction-diffusion models for action potential propagation in the human heart. IEEE Transactions on Biomedical Engineering 53: 2425-2435.
64. Luo CH, Rudy Y, (1994) A dynamic model of the cardiac ventricular action potential. I. Simulations of ionic currents and concentration changes. Circ. Res 74: 1071-1096.
65. Luo CH, Rudy Y, (1994) A dynamic model of the cardiac ventricular action potential. II. Afterdepolarizations, triggered activity, and potentiation. Circ. Res 74: 1097-1113.
66. Bernus O, Wilders R, Zemlin CW, Versschelde H, Panfilov AV, (2002) A computationally efficient electro-physiological model of human ventricular cells. Am J Physiol Heart Circ Physiol 282: H2296.
67. Ferencik M, Abbara S, Hoffmann U, Cury RC, Brady TJ, et al. (2004) Left Ventricular Thin-Point Detection Using Multidetector Spiral Computed Tomography. The American Journal of Cardiology 93 April 1.
68. Wu TJ, Lin SF, Weiss JN, Ting CT, Chen PS, (2002) Two types of ventricular fibrillation in isolated rabbit hearts: importance of excitability and action potential duration restitution. Circulation 106 (14): 1859-66.
69. Clusin WT, Bristow MR, Baim DS, Schroeder JS, Jaillon P, et al. (1982) The effects of diltiazem and reduced serum ionized calcium on ischemic ventricular fibrillation in the dog. Circ Res 50 (4): 518-26.
70. Nearing BD, Hutter JJ, Verrier RL, (1996) Potent antifibrillatory effect of combined blockade of calcium channels and 5-HT2 receptors with nexopamil during myocardial ischemia and reperfusion in dogs: comparison to diltiazem. J Cardiovasc Pharmacol 27 (6): 777-87.