Pro-arrhythmogenic effects of atrial fibrillation-induced electrical remodelling: Insights from the three-dimensional virtual human atria

Journal of Physiology

Volumn 591, Issue 17, 2013, Pages 4249-4272

  Colman, Michael A ^a   Aslanidi, Oleg V ^a,b   Kharche, Sanjay ^a   Boyett, Mark R ^a   Garratt, Clifford ^c   Hancox, Jules C ^d   Zhang, Henggui ^a,e  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c MANCHESTER ROYAL INFIRMARY   (United Kingdom)

^d SCHOOL OF MEDICAL SCIENCES   (United Kingdom)

^e HARBIN INSTITUTE OF TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL L TYPE; DELAYED RECTIFIER POTASSIUM CHANNEL; ION CHANNEL; SODIUM CALCIUM EXCHANGE PROTEIN;

ACTION POTENTIAL; ACTION POTENTIAL DURATION; ACTION POTENTIAL PROFILE; ARRHYTHMOGENESIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM CHANNEL L TYPE CURRENT; CELL HETEROGENEITY; COMPUTER MODEL; HEART ATRIUM; HEART ATRIUM FIBRILLATION; HEART ATRIUM FIBRILLATION INDUCED ELECTRICAL REMODELLING; HEART ELECTROPHYSIOLOGY; HEART RHYTHM; HEART STIMULATION; INWARD RECTIFIER POTASSIUM CHANNEL CURRENT; ION CURRENT; L TYPE CALCIUM CHANNEL CURRENT; MEMBRANE CURRENT; MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN INTERACTION; RECURRENT DISEASE; SIMULATION; SLOW DELAYED RECTIFIER POTASSIUM CHANNEL CURRENT; SODIUM CALCIUM EXCHANGER CURRENT; THREE DIMENSIONAL IMAGING; TRANSIENT OUTWARD POTASSIUM CHANNEL CURRENT; ULTRA RAPID DELAYED RECTIFIER POTASSIUM CHANNEL CURRENT; BIOLOGICAL MODEL; CYTOLOGY; HEART ATRIUM REMODELING; HEART MUSCLE CELL; HUMAN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ATRIAL FIBRILLATION; ATRIAL REMODELING; HEART ATRIA; HUMANS; ION CHANNELS; MODELS, CARDIOVASCULAR; MYOCYTES, CARDIAC;

EID: 84883270078     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.254987     Document Type: Article

References (99)

1. Allessie MA, Bonke FI & Schopman FJ (1976). Circus movement in rabbit atrial muscle as a mechanism of tachycardia. II. The role of nonuniform recovery of excitability in the occurrence of unidirectional block, as studied with multiple microelectrodes. Circ Res 39, 168-177.
2. Anter E, Jessup M & Callans DJ (2009). Atrial fibrillation and heart failure: treatment considerations for a dual epidemic. Circulation 119, 2516-2525.
3. Arora R, Verheule S, Scott L, Navarrete A, Katari V, Wilson E, Vaz D & Olgin JE (2003). Arrhythmogenic substrate of the pulmonary veins assessed by high-resolution optical mapping. Circulation 107, 1816-1821.
4. Aslanidi OV, Boyett MR, Dobrzynski H, Li J & Zhang H (2009). Mechanisms of transition from normal to reentrant electrical activity in a model of rabbit atrial tissue: interaction of tissue heterogeneity and anisotropy. Biophys J 96, 798-817.
5. Aslanidi OV, Butters TD, Ren CX, Ryecroft G & Zhang H (2011a). Electrophysiological models for the heterogeneous canine atria: computational platform for studying rapid atrial arrhythmias. Conf Proc IEEE Eng Med Biol Soc 2012, 1693-1696.
6. Aslanidi OV, Colman MA, Stott J, Dobrzynski H, Boyett MR, Holden AV & Zhang H (2011b). 3D virtual human atria: a computational platform for studying clinical atrial fibrillation. Prog Biophys Mol Biol 107, 156-168.
7. Aslanidi OV, Colman MA, Varela M, Zhao J, Smaill BH, Hancox JC, Boyett MR & Zhang H (2013a). Heterogeneous and anisotropic integrative model of pulmonary veins: computational study of arrhythmogenic substrate for atrial fibrillation. Interface Focus doi: 10.1098/rsfs.2012.0069. http://rsfs.royalsocietypublishing.org/content/3/2/20120069.abstract.
8. Aslanidi OV, Nikolaidou T, Zhao J, Smaill BH, Gilbert SH, Holden AV, Lowe T, Withers PJ, Stephenson RS, Jarvis JC, Hancox JC, Boyett MR & Zhang H (2013b). Application of micro-computed tomography with iodine staining to cardiac imaging, segmentation, and computational model development. IEEE Trans Med Imaging 32, 8-17.
9. Ausma J, Wijffels M, Van Eys G, Koide M, Ramaekers F, Allessie M & Borgers M (1997a). Dedifferentiation of atrial cardiomyocytes as a result of chronic atrial fibrillation. Am J Pathol 151, 985-997.
10. Ausma J, Wijffels M, Thoné F, Wouters L, Allessie M & Borgers M (1997b). Structural changes of atrial myocardium due to sustained atrial fibrillation in the goat. Circulation 96, 3157-3163.
11. Benjamin EJ, Wolf PA, D'Agostino RB, Silbershatz H, Kannel WB & Levy D (1998). Impact of atrial fibrillation on the risk of death: the Framingham Heart Study. Circulation 98, 946-952.
12. Benson AP, Aslanidi OV, Zhang H & Holden AV (2008). The canine virtual ventricular wall: a platform for dissecting pharmacological effects on propagation and arrhythmogenesis. Prog Biophys Mol Biol 96, 187-208.
13. Bikou O, Thomas D, Trappe K, Lugenbiel P, Kelemen K, Koch M, Soucek R, Voss F, Becker R, Katus HA & Bauer A (2011). Connexin 43 gene therapy prevents persistent atrial fibrillation in a porcine model. Cardiovasc Res 92, 218-225.
14. Boineau JP, Canavan TE, Schuessler RB, Cain ME, Corr PB & Cox JL (1988). Demonstration of a widely distributed atrial pacemaker complex in the human heart. Circulation 77, 1221-1237.
15. Bosch RF, Zeng X, Grammer JB, Popovic K, Mewis C & Kühlkamp V (1999). Ionic mechanisms of electrical remodeling in human atrial fibrillation. Cardiovasc Res 44, 121-131.
16. + current in human atrial fibrillation. Their possible role in postoperative atrial fibrillation. J Mol Cell Cardiol 32, 1885-1896.
17. Brundel BJ, Van Gelder IC, Henning RH, Tieleman RG, Tuinenburg AE, Wietses M, Grandjean JG, Van Gilst WH & Crijns HJ (2001a). Ion channel remodeling is related to intraoperative atrial effective refractory periods in patients with paroxysmal and persistent atrial fibrillation. Circulation 103, 684-690.
18. + channels. J Am Coll Cardiol 37, 926-932.
19. Kur promote atrial fibrillation Heart Rhythm 5, 1304-1309.
20. Kur/Ito block. Am J Physiol Heart Circ Physiol 286, H2393-2400.
21. Butters TD, Aslanidi OV, Zhao J, Smaill B & Zhang H (2013). A novel computational sheep atria model for the study of atrial fibrillation. Interface Focus doi: 10.1098/rsfs.2012.0067.
22. Caballero R, De la Fuente MG, Gómez R, Barana A, Amorós I, Dolz-Gaitón P, Osuna L, Almendral J, Atienza F, Fernández-Avilés F, Pita A, Rodríguez-Roda J, Pinto A, Tamargo J & Delpón E (2010). In humans, chronic atrial fibrillation decreases the transient outward current and ultrarapid component of the delayed rectifier current differentially on each atria and increases the slow component of the delayed rectifier current in both. J Am Coll Cardiol 55, 2346-2354.
23. Calkins H et al. (2012). 2012 HRS/EHRA/ECAS Expert Consensus Statement on Catheter and Surgical Ablation of Atrial Fibrillation: recommendations for patient selection, procedural techniques, patient management and follow-up, definitions, endpoints, and research trial design. Europace 14, 528-606.
24. Camm AJ et al. (2010). Guidelines for the management of atrial fibrillation: the Task Force for the Management of Atrial Fibrillation of the European Society of Cardiology (ESC). Europace 12, 1360-1420.
25. Chandler N, Aslanidi O, Buckley D, Inada S, Birchall S, Atkinson A, Kirk D, Monfredi O, Molenaar P, Anderson R, Sharma V, Sigg D, Zhang H, Boyett M & Dobrzynski H (2011). Computer three-dimensional anatomical reconstruction of the human sinus node and a novel paranodal area. Anat Rec (Hoboken) 294, 970-979.
26. Chen SA, Hsieh MH, Tai CT, Tsai CF, Prakash VS, Yu WC, Hsu TL, Ding YA & Chang MS (1999). 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.
27. 2+ current downregulation in chronic human atrial fibrillation is associated with increased activity of protein phosphatases. Circulation 110, 2651-2657.
28. K, ACh blocker AVE0118 on ion channels in human chronic atrial fibrillation. Br J Pharmacol 154, 1619-1630.
29. Clayton RH, Bernus O, Cherry EM, Dierckx H, Fenton FH, Mirabella L, Panfilov AV, Sachse FB, Seemann G & Zhang H (2011). Models of cardiac tissue electrophysiology: progress, challenges and open questions. Prog Biophys Mol Biol 104, 22-48.
30. Colman MA, Aslanidi OV, Stott J, Holden AV & Zhang H (2011). Correlation between P-wave morphology and origin of atrial focal tachycardia-insights from realistic models of the human atria and torso. IEEE Trans Biomed Eng 58, 2952-2955.
31. Courtemanche M, Ramirez RJ & Nattel S (1998). Ionic mechanisms underlying human atrial action potential properties: insights from a mathematical model. Am J Physiol 275, H301-321.
32. Cox JL, Canavan TE, Schuessler RB, Cain ME, Lindsay BD, Stone C, Smith PK, Corr PB & Boineau JP ((1991). The surgical treatment of atrial fibrillation. II. Intraoperative electrophysiologic mapping and description of the electrophysiologic basis of atrial flutter and atrial fibrillation. J Thorac Cardiovasc Surg 101, 406-426.
33. Dawodu AA, Monti F, Iwashiro K, Schiariti M, Chiavarelli R & Puddu PE (1996). The shape of human atrial action potential accounts for different frequency-related changes in vitro. Int J Cardiol 54, 237-249.
34. K, ACh and muscarinic receptor-mediated shortening of action potentials. Circulation 104, 2551-2557.
35. Dobrev D & Ravens U (2003). Remodeling of cardiomyocyte ion channels in human atrial fibrillation. Basic Res Cardiol 98, 137-148.
36. Dobrev D, Wettwer E, Kortner A, Knaut M, Schüler S & Ravens U (2002). Human inward rectifier potassium channels in chronic and postoperative atrial fibrillation. Cardiovasc Res 54, 397-404.
37. Dorn A, Krueger MW, Seemann G & Doessel O (2012). Modelling of heterogeneous human atrial electrophysiology. Biomed Tech (Berl) doi: 10.1515/bmt-2012-4215.
38. Dössel O, Krueger MW, Weber FM, Wilhelms M & Seemann G (2012). Computational modelling of the human atrial anatomy and electrophysiology. Med Biol Eng Comput 50, 773-799.
39. Ehrlich JR, Cha T-J, Zhang L, Chartier D, Melnyk P, Hohnloser SH & Nattel S (2003). Cellular electrophysiology of canine pulmonary vein cardiomyocytes: action potential and ionic current properties. J Physiol 551, 801-813.
40. 2+ handling in human chronic atrial fibrillation. Circulation 114, 670-680.
41. Fareh S, Villemaire C & Nattel S (1998). Importance of refractoriness heterogeneity in the enhanced vulnerability to atrial fibrillation induction caused by tachycardia-induced atrial electrical remodeling. Circulation 98, 2202-2209.
42. Fedorov VV, Ambrosi CM, Kostecki G, Hucker WJ, Glukhov AV, Wuskell JP, Loew LM, Moazami N & Efimov IR (2011). Anatomic localization and autonomic modulation of atrioventricular junctional rhythm in failing human hearts. Circ Arrhythm Electrophysiol 4, 515-525.
43. Feng J, Yue L, Wang Z & Nattel S (1998). Ionic mechanisms of regional action potential heterogeneity in the canine right atrium. Circ Res 83, 541-551.
44. De la Fuente MG, Barana A, Gómez R, Amorós I, Dolz-Gaitón P, Sacristán S, Atienza F, Pita A, Pinto Á, Fernández-Avilés F, Caballero R, Tamargo J & Delpón E (2013). Chronic atrial fibrillation up-regulates β1-adrenoceptors affecting repolarizing currents and action potential duration. Cardiovasc Res 97, 379-388.
45. 2+ currents between myocytes from human atrial right appendage and atrial septum. Cell Physiol Biochem 21, 385-394.
46. Grammer JB, Bosch RF, Kühlkamp V & Seipel L (2000). Molecular remodeling of Kv4.3 potassium channels in human atrial fibrillation. J Cardiovasc Electrophysiol 11, 626-633.
47. 2+ model: sinus rhythm and chronic atrial fibrillation. Circ Res 109, 1055-1066.
48. Haïssaguerre M, Jaïs P, Shah DC, Takahashi A, Hocini M, Quiniou G, Garrigue S, Le Mouroux A, Le Métayer P & Clémenty J (1998). Spontaneous initiation of atrial fibrillation by ectopic beats originating in the pulmonary veins. N Engl J Med 339, 659-666.
49. Harada A, Sasaki K, Fukushima T, Ikeshita M, Asano T, Yamauchi S, Tanaka S & Shoji T (1996). Atrial activation during chronic atrial fibrillation in patients with isolated mitral valve disease. Ann Thorac Surg 61, 104-111; discussion 111-112.
50. Ho SY, Anderson RH & Sánchez-Quintana D (2002). Atrial structure and fibres: morphologic bases of atrial conduction. Cardiovasc Res 54, 325-336.
51. Hove-Madsen L, Llach A, Bayes-Genís A, Roura S, Rodriguez Font E, Arís A & Cinca J (2004). Atrial fibrillation is associated with increased spontaneous calcium release from the sarcoplasmic reticulum in human atrial myocytes. Circulation 110, 1358-1363.
52. Hsu N-W, Lin Y-J, Tai C-T, Kao T, Chang S-L, Wongcharoen W, Lo L-W, Udyavar AR, Hu Y-F, Tso H-W, Chen Y-J, Higa S & Chen S-A (2008). Frequency analysis of the fibrillatory activity from surface ECG lead V1 and intracardiac recordings: implications for mapping of AF. Europace 10, 438-443.
53. Jalife J, Berenfeld O & Mansour M (2002). Mother rotors and fibrillatory conduction: a mechanism of atrial fibrillation. Cardiovasc Res 54, 204-216.
54. Jones G, Spencer BD, Adeniran I & Zhang H (2012). Development of biophysically detailed electrophysiological models for pacemaking and non-pacemaking human pulmonary vein cardiomyocytes. Conf Proc IEEE Eng Med Biol Soc 2012, 199-202.
55. Katoh H, Shinozaki T, Baba S, Satoh S, Kagaya Y, Watanabe J & Shirato K (2005). Monophasic action potential duration at the crista terminalis in patients with sinus node disease. Circ J 69, 1361-1367.
56. Kharche S, Adeniran I, Stott J, Law P, Boyett MR, Hancox JC & Zhang H (2012). Pro-arrhythmogenic effects of the S140G KCNQ1 mutation in human atrial fibrillation - insights from modelling. J Physiol 590, 4501-4514.
57. K1) arising from KCNJ2 mutation-a simulation study. Prog Biophys Mol Biol 98, 186-197.
58. Kharche S & Zhang H (2008). Simulating the effects of atrial fibrillation induced electrical remodeling: a comprehensive simulation study. Conf Proc IEEE Eng Med Biol Soc 2008, 593-596.
59. Koivumäki JT, Korhonen T & Tavi P (2011). Impact of sarcoplasmic reticulum calcium release on calcium dynamics and action potential morphology in human atrial myocytes: a computational study. PLoS Comput Biol 7, e1001067.
60. Kumagai K, Ogawa M, Noguchi H, Yasuda T, Nakashima H & Saku K (2004). Electrophysiologic properties of pulmonary veins assessed using a multielectrode basket catheter. J Am Coll Cardiol 43, 2281-2289.
61. Lai LP, Su MJ, Lin JL, Lin FY, Tsai CH, Chen YS, Tseng YZ, Lien WP & Huang SK (1999). Changes in the mRNA levels of delayed rectifier potassium channels in human atrial fibrillation. Cardiology 92, 248-255.
62. Lemery R, Birnie D, Tang ASL, Green M, Gollob M, Hendry M & Lau E (2007). Normal atrial activation and voltage during sinus rhythm in the human heart: an endocardial and epicardial mapping study in patients with a history of atrial fibrillation. J Cardiovasc Electrophysiol 18, 402-408.
63. Li D, Zhang L, Kneller J & Nattel S (2001). Potential ionic mechanism for repolarization differences between canine right and left atrium. Circ Res 88, 1168-1175.
64. + current changes account for the rate dependence of the action potential in the human atrial myocyte. Am J Physiol Heart Circ Physiol 297, H1398-1410.
65. Mandapati R, Skanes A, Chen J, Berenfeld O & Jalife J (2000). Stable microreentrant sources as a mechanism of atrial fibrillation in the isolated sheep heart. Circulation 101, 194-199.
66. Mansour M, Mandapati R, Berenfeld O, Chen J, Samie FH & Jalife J (2001). Left-to-right gradient of atrial frequencies during acute atrial fibrillation in the isolated sheep heart. Circulation 103, 2631-2636.
67. McDowell KS, Vadakkumpadan F, Blake R, Blauer J, Plank G, MacLeod RS & Trayanova NA (2012). Methodology for patient-specific modelling of atrial fibrosis as a substrate for atrial fibrillation. J Electrocardiol 45, 640-645.
68. Morillo CA, Klein GJ, Jones DL & Guiraudon CM (1995). Chronic rapid atrial pacing. Structural, functional, and electrophysiological characteristics of a new model of sustained atrial fibrillation. Circulation 91, 1588-1595.
69. Nattel S, Shiroshita-Takeshita A, Brundel BJJM & Rivard L (2005). Mechanisms of atrial fibrillation: lessons from animal models. Prog Cardiovasc Dis 48, 9-28.
70. 2+ levels in right atrial myocardium of patients with atrial fibrillation. Circ Res 106, 1134-1144.
71. Oh S, Kim K-B, Ahn H, Cho H-J & Choi Y-S (2010). Remodeling of ion channel expression in patients with chronic atrial fibrillation and mitral valvular heart disease. Korean J Intern Med 25, 377-385.
72. Pandit SV, Berenfeld O, Anumonwo JMB, Zaritski RM, Kneller J, Nattel S & Jalife J (2005). Ionic determinants of functional reentry in a 2-D model of human atrial cells during simulated chronic atrial fibrillation. Biophys J 88, 3806-3821.
73. Polontchouk L, Haefliger JA, Ebelt B, Schaefer T, Stuhlmann D, Mehlhorn U, Kuhn-Regnier F, De Vivie ER & Dhein S (2001). Effects of chronic atrial fibrillation on gap junction distribution in human and rat atria. J Am Coll Cardiol 38, 883-891.
74. Ridler M-E, Lee M, McQueen D, Peskin C & Vigmond E (2011). Arrhythmogenic consequences of action potential duration gradients in the atria. Can J Cardiol 27, 112-119.
75. Rosanio S, Ware DL & Saeed M (2004). Pulmonary vein ablation of atrial fibrillation: beyond the traditional. Am J Med Sci 328, 323-329.
76. Sanders P, Berenfeld O, Hocini M, Jaïs P, Vaidyanathan R, Hsu L-F, Garrigue S, Takahashi Y, Rotter M, Sacher F, Scavée C, Ploutz-Snyder R, Jalife J & Haïssaguerre M (2005). Spectral analysis identifies sites of high-frequency activity maintaining atrial fibrillation in humans. Circulation 112, 789-797.
77. Schotten U, Greiser M, Benke D, Buerkel K, Ehrenteidt B, Stellbrink C, Vazquez-Jimenez JF, Schoendube F, Hanrath P & Allessie M (2002). Atrial fibrillation-induced atrial contractile dysfunction: a tachycardiomyopathy of a different sort. Cardiovasc Res 53, 192-201.
78. Seemann G, Höper C, Sachse FB, Dössel O, Holden AV & Zhang H (2006). Heterogeneous three-dimensional anatomical and electrophysiological model of human atria. Philos Trans A Math Phys Eng Sci 364, 1465-1481.
79. Severs NJ, Bruce AF, Dupont E & Rothery S (2008). Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res 80, 9-19.
80. Severs NJ, Coppen SR, Dupont E, Yeh H-I, Ko Y-S & Matsushita T (2004). Gap junction alterations in human cardiac disease. Cardiovasc Res 62, 368-377.
81. 2+ uptake in human atrial fibrillation. Biochem Biophys Res Commun 410, 97-101.
82. Skasa M, Jüngling E, Picht E, Schöndube F & Lückhoff A (2001). L-type calcium currents in atrial myocytes from patients with persistent and non-persistent atrial fibrillation. Basic Res Cardiol 96, 151-159.
83. Spach MS, Dolber PC & Heidlage JF (1989). Interaction of inhomogeneities of repolarization with anisotropic propagation in dog atria. A mechanism for both preventing and initiating reentry. Circ Res 65, 1612-1631.
84. Stewart S, Murphy NF, Murphy N, Walker A, McGuire A & McMurray JJV (2004). Cost of an emerging epidemic: an economic analysis of atrial fibrillation in the UK. Heart 90, 286-292.
85. Sun H, Gaspo R, Leblanc N & Nattel S (1998). Cellular mechanisms of atrial contractile dysfunction caused by sustained atrial tachycardia. Circulation 98, 719-727.
86. Van der Velden HMW & Jongsma HJ (2002). Cardiac gap junctions and connexins: their role in atrial fibrillation and potential as therapeutic targets. Cardiovasc Res 54, 270-279.
87. van Wagoner DR & Nerbonne JM (2000). Molecular basis of electrical remodeling in atrial fibrillation. J Mol Cell Cardiol 32, 1101-1117.
88. 2+ currents and human atrial fibrillation. Circ Res 85, 428-436.
89. + current densities and Kv1.5 expression are reduced in chronic human atrial fibrillation. Circ Res 80, 772-781.
90. 2+ exchanger function underlie delayed afterdepolarizations in patients with chronic atrial fibrillation. Circulation 125, 2059-2070.
91. Weerasooriya R, Khairy P, Litalien J, Macle L, Hocini M, Sacher F, Lellouche N, Knecht S, Wright M, Nault I, Miyazaki S, Scavee C, Clementy J, Haissaguerre M & Jais P (2011). Catheter ablation for atrial fibrillation: are results maintained at 5 years of follow-up J Am Coll Cardiol 57, 160-166.
92. Kur in controlling action potential shape and contractility in the human atrium influence of chronic atrial fibrillation. Circulation 110, 2299-2306.
93. Wilhelms M, Hettmann H, Maleckar MM, Koivumäki JT, Dössel O & Seemann G (2012). Benchmarking electrophysiological models of human atrial myocytes. Front Physiol 3, 487.
94. Workman AJ, Kane KA & Rankin AC (2001). The contribution of ionic currents to changes in refractoriness of human atrial myocytes associated with chronic atrial fibrillation. Cardiovasc Res 52, 226-235.
95. Workman AJ, Pau D, Redpath CJ, Marshall GE, Russell JA, Norrie J, Kane KA & Rankin AC (2009). Atrial cellular electrophysiological changes in patients with ventricular dysfunction may predispose to AF. Heart Rhythm 6, 445-451.
96. Yamazaki M, Mironov S, Taravant C, Brec J, Vaquero LM, Bandaru K, Avula UMR, Honjo H, Kodama I, Berenfeld O & Kalifa J (2012). Heterogeneous atrial wall thickness and stretch promote scroll waves anchoring during atrial fibrillation. Cardiovasc Res 94, 48-57.
97. Zhang H, Garratt CJ, Kharche S & Holden AV (2009). Remodelling of cellular excitation (reaction) and intercellular coupling (diffusion) by chronic atrial fibrillation represented by a reaction-diffusion system. Physica D 238, 976-983.
98. K1 in action potential shortening associated with atrial fibrillation in humans. Cardiovasc Res 66, 493-502.
99. Zhao J, Butters TD, Zhang H, Legrice IJ, Sands GB & Smaill BH (2013). Image-based model of atrial anatomy and electrical activation: a computational platform for investigating atrial arrhythmia. IEEE Trans Med Imaging 32, 18-27.