Progression and reversibility of stretch induced atrial remodeling: Characterization and clinical implications

Progress in Biophysics and Molecular Biology

Volumn 130, Issue , 2017, Pages 376-386

  Thanigaimani, Shivshankar ^a   McLennan, Emma ^a   Linz, Dominik ^a   Mahajan, Rajiv ^a   Agbaedeng, Thomas A ^a   Lee, Geoffrey ^b   Kalman, Jonathan M ^b   Sanders, Prashanthan ^a   Lau, Dennis H ^a  

^a ROYAL ADELAIDE HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BIOMECHANICS; HEART ATRIUM REMODELING; HUMAN; MECHANICS;

ANIMALS; ATRIAL REMODELING; BIOMECHANICAL PHENOMENA; HUMANS; MECHANICAL PHENOMENA;

EID: 85026371339     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2017.07.010     Document Type: Review

References (108)

1. Abed, H.S., Samuel, C.S., Lau, D.H., Kelly, D.J., Royce, S.G., Alasady, M., Mahajan, R., Kuklik, P., Zhang, Y., Brooks, A.G., Nelson, A.J., Worthley, S.G., Abhayaratna, W.P., Kalman, J.M., Wittert, G.A., Sanders, P., Obesity results in progressive atrial structural and electrical remodeling: implications for atrial fibrillation. Heart Rhythm 10 (2013), 90–100.
2. Abed, H.S., Wittert, G.A., Leong, D.P., Shirazi, M.G., Bahrami, B., Middeldorp, M.E., Lorimer, M.F., Lau, D.H., Antic, N.A., Brooks, A.G., Abhayaratna, W.P., Kalman, J.M., Sanders, P., Effect of weight reduction and cardiometabolic risk factor management on symptom burden and severity in patients with atrial fibrillation: a randomized clinical trial. JAMA 310 (2013), 2050–2060.
3. Anderson, R.H., Ho, S.Y., “Specialized” conducting cells in the pulmonary veins. J. Cardiovasc Electrophysiol., 15, 2004, 121 author reply 121–123.
4. Andrade, J., Khairy, P., Dobrev, D., Nattel, S., The clinical profile and pathophysiology of atrial fibrillation: relationships among clinical features, epidemiology, and mechanisms. Circ. Res. 114 (2014), 1453–1468.
5. Anne, W., Willems, R., Holemans, P., Beckers, F., Roskams, T., Lenaerts, I., Ector, H., Heidbuchel, H., Self-terminating AF depends on electrical remodeling while persistent AF depends on additional structural changes in a rapid atrially paced sheep model. J. Mol. Cell Cardiol. 43 (2007), 148–158.
6. Antoniou, A., Milonas, D., Kanakakis, J., Rokas, S., Sideris, D.A., Contraction-excitation feedback in human atrial fibrillation. Clin. Cardiol. 20 (1997), 473–476.
7. Bainbridge, F.A., The influence of venous filling upon the rate of the heart. J. Physiol. 50 (1915), 65–84.
8. Benjamin, E.J., Chen, P.S., Bild, D.E., Mascette, A.M., Albert, C.M., Alonso, A., Calkins, H., Connolly, S.J., Curtis, A.B., Darbar, D., Ellinor, P.T., Go, A.S., Goldschlager, N.F., Heckbert, S.R., Jalife, J., Kerr, C.R., Levy, D., Lloyd-Jones, D.M., Massie, B.M., Nattel, S., Olgin, J.E., Packer, D.L., Po, S.S., Tsang, T.S., Van Wagoner, D.R., Waldo, A.L., Wyse, D.G., Prevention of atrial fibrillation: report from a national heart, lung, and blood institute workshop. Circulation 119 (2009), 606–618.
9. Bode, F., Katchman, A., Woosley, R.L., Franz, M.R., Gadolinium decreases stretch-induced vulnerability to atrial fibrillation. Circulation 101 (2000), 2200–2205.
10. Boyden, P.A., Hoffman, B.F., The effects on atrial electrophysiology and structure of surgically induced right atrial enlargement in dogs. Circ. Res. 49 (1981), 1319–1331.
11. Brunner, F., Mouton, R., Lochner, A., Opie, L.H., Defective stretch-induced release of atrial natriuretic peptide from aging hypertensive rat heart: possible role of phosphatidylinositol pathway. J. Cardiovasc. Pharmacol. 25 (1995), 168–176.
12. Calkins, H., el-Atassi, R., Kalbfleisch, S., Langberg, J., Morady, F., Effects of an acute increase in atrial pressure on atrial refractoriness in humans. Pacing Clin. Electrophysiol. 15 (1992), 1674–1680.
13. Calkins, H., el-Atassi, R., Leon, A., Kalbfleisch, S., Borganelli, M., Langberg, J., Morady, F., Effect of the atrioventricular relationship on atrial refractoriness in humans. Pacing Clin. Electrophysiol. 15 (1992), 771–778.
14. Cardin, S., Li, D., Thorin-Trescases, N., Leung, T.K., Thorin, E., Nattel, S., Evolution of the atrial fibrillation substrate in experimental congestive heart failure: angiotensin-dependent and -independent pathways. Cardiovasc. Res. 60 (2003), 315–325.
15. Cha, T.-J., Ehrlich, J.R., Zhang, L., Shi, Y.-F., Tardif, J.-C., Leung, T.K., Nattel, S., Dissociation between ionic remodeling and ability to sustain atrial fibrillation during recovery from experimental congestive heart failure. Circulation 109 (2004), 412–418.
16. Cha, T.J., Ehrlich, J.R., Zhang, L., Nattel, S., Atrial ionic remodeling induced by atrial tachycardia in the presence of congestive heart failure. Circulation 110 (2004), 1520–1526.
17. Chen, Y.J., Tai, C.T., Chiou, C.W., Wen, Z.C., Chan, P., Lee, S.H., Chen, S.A., Inducibility of atrial fibrillation during atrioventricular pacing with varying intervals: role of atrial electrophysiology and the autonomic nervous system. J. Cardiovasc. Electrophysiol. 10 (1999), 1578–1585.
18. Choisy, S.C., Arberry, L.A., Hancox, J.C., James, A.F., Increased susceptibility to atrial tachyarrhythmia in spontaneously hypertensive rat hearts. Hypertension 49 (2007), 498–505.
19. Dimitri, H., Ng, M., Brooks, A.G., Kuklik, P., Stiles, M.K., Lau, D.H., Antic, N., Thornton, A., Saint, D.A., McEvoy, D., Antic, R., Kalman, J.M., Sanders, P., Atrial remodeling in obstructive sleep apnea: implications for atrial fibrillation. Heart Rhythm 9 (2012), 321–327.
20. Eijsbouts, S.C., Houben, R.P., Blaauw, Y., Schotten, U., Allessie, M.A., Synergistic action of atrial dilation and sodium channel blockade on conduction in rabbit atria. J. Cardiovasc. Electrophysiol. 15 (2004), 1453–1461.
21. Eijsbouts, S.C., Majidi, M., van Zandvoort, M., Allessie, M.A., Effects of acute atrial dilation on heterogeneity in conduction in the isolated rabbit heart. J. Cardiovasc. Electrophysiol. 14 (2003), 269–278.
22. Elvan, A., Adiyaman, A., Beukema, R.J., Sie, H.T., Allessie, M.A., Electrophysiological effects of acute atrial stretch on persistent atrial fibrillation in patients undergoing open heart surgery. Heart Rhythm 10 (2013), 322–330.
23. Fan, K., Lee, K.L., Chow, W.H., Chau, E., Lau, C.P., Internal cardioversion of chronic atrial fibrillation during percutaneous mitral commissurotomy: insight into reversal of chronic stretch-induced atrial remodeling. Circulation 105 (2002), 2746–2752.
24. Franz, M.R., Bode, F., Mechano-electrical feedback underlying arrhythmias: the atrial fibrillation case. Prog. Biophys. Mol. Biol. 82 (2003), 163–174.
25. Frost, L., Hune, L.J., Vestergaard, P., Overweight and obesity as risk factors for atrial fibrillation or flutter: the Danish diet, cancer, and health study. Am. J. Med. 118 (2005), 489–495.
26. Gami, A.S., Hodge, D.O., Herges, R.M., Olson, E.J., Nykodym, J., Kara, T., Somers, V.K., Obstructive sleep apnea, obesity, and the risk of incident atrial fibrillation. J. Am. Coll. Cardiol. 49 (2007), 565–571.
27. Gami, A.S., Pressman, G., Caples, S.M., Kanagala, R., Gard, J.J., Davison, D.E., Malouf, J.F., Ammash, N.M., Friedman, P.A., Somers, V.K., Association of atrial fibrillation and obstructive sleep apnea. Circulation 110 (2004), 364–367.
28. Gao, S., Park, B.M., Cha, S.A., Park, W.H., Park, B.H., Kim, S.H., Angiotensin AT2 receptor agonist stimulates high stretch induced- ANP secretion via PI3K/NO/sGC/PKG/pathway. Peptides 47 (2013), 36–44.
29. Goette, A., Kalman, J.M., Aguinaga, L., Akar, J., Cabrera, J.A., Chen, S.A., Chugh, S.S., Corradi, D., D'Avila, A., Dobrev, D., Fenelon, G., Gonzalez, M., Hatem, S.N., Helm, R., Hindricks, G., Ho, S.Y., Hoit, B., Jalife, J., Kim, Y.H., Lip, G.Y., Ma, C.S., Marcus, G.M., Murray, K., Nogami, A., Sanders, P., Uribe, W., Van Wagoner, D.R., Nattel, S., EHRA/HRS/APHRS/SOLAECE expert consensus on atrial cardiomyopathies: definition, characterization, and clinical implication. Heart Rhythm 14 (2017), e3–e40.
30. Goudis, C.A., Kallergis, E.M., Vardas, P.E., Extracellular matrix alterations in the atria: insights into the mechanisms and perpetuation of atrial fibrillation. Europace 14 (2012), 623–630.
31. Harrison, J.L., Jensen, H.K., Peel, S.A., Chiribiri, A., Grøndal, A.K., Bloch, L.Ø., Pedersen, S.F., Bentzon, J.F., Kolbitsch, C., Karim, R., Williams, S.E., Linton, N.W., Rhode, K.S., Gill, J., Cooklin, M., Rinaldi, C.A., Wright, M., Kim, W.Y., Schaeffter, T., Razavi, R.S., O'Neill, M.D., Cardiac magnetic resonance and electroanatomical mapping of acute and chronic atrial ablation injury: a histological validation study. Eur. Heart J. 35 (2014), 1486–1495.
32. Haugan, K., Miyamoto, T., Takeishi, Y., Kubota, I., Nakayama, J., Shimojo, H., Hirose, M., Rotigaptide (ZP123) improves atrial conduction slowing in chronic volume overload-induced dilated atria. Basic Clin. Pharmacol. Toxicol. 99 (2006), 71–79.
33. Hirose, M., Takeishi, Y., Miyamoto, T., Kubota, I., Laurita, K.R., Chiba, S., Mechanism for atrial tachyarrhythmia in chronic volume overload-induced dilated atria. J. Cardiovasc. Electrophysiol. 16 (2005), 760–769.
34. Hunter, R.J., Liu, Y., Lu, Y., Wang, W., Schilling, R.J., Left atrial wall stress distribution and its relationship to electrophysiologic remodeling in persistent atrial fibrillation. Circ. Arrhythm. Electrophysiol. 5 (2012), 351–360.
35. John, B., Stiles, M.K., Kuklik, P., Brooks, A.G., Chandy, S.T., Kalman, J.M., Sanders, P., Reverse remodeling of the atria after treatment of chronic stretch in humans: implications for the atrial fibrillation substrate. J. Am. Coll. Cardiol. 55 (2010), 1217–1226.
36. Kalifa, J., Bernard, M., Gout, B., Bril, A., Cozma, D., Laurent, P., Chalvidan, T., Deharo, J.C., Djiane, P., Cozzone, P., Maixent, J.M., Anti-arrhythmic effects of I (Na), I (Kr), and combined I (Kr)-I (CaL) blockade in an experimental model of acute stretch-related atrial fibrillation. Cardiovasc Drugs Ther. 21 (2007), 47–53.
37. Kalifa, J., Jalife, J., Zaitsev, A.V., Bagwe, S., Warren, M., Moreno, J., Berenfeld, O., Nattel, S., Intra-atrial pressure increases rate and organization of waves emanating from the superior pulmonary veins during atrial fibrillation. Circulation 108 (2003), 668–671.
38. Kamkin, A., Kiseleva, I., Lozinsky, I., Scholz, H., Electrical interaction of mechanosensitive fibroblasts and myocytes in the heart. Basic Res. Cardiol. 100 (2005), 337–345.
39. Kanagala, R., Murali, N.S., Friedman, P.A., Ammash, N.M., Gersh, B.J., Ballman, K.V., Shamsuzzaman, A.S., Somers, V.K., Obstructive sleep apnea and the recurrence of atrial fibrillation. Circulation 107 (2003), 2589–2594.
40. Kaseda, S., Zipes, D.P., Contraction-excitation feedback in the atria: a cause of changes in refractoriness. J. Am. Coll. Cardiol. 11 (1988), 1327–1336.
41. Kistler, P.M., Sanders, P., Dodic, M., Spence, S.J., Samuel, C.S., Zhao, C., Charles, J.A., Edwards, G.A., Kalman, J.M., Atrial electrical and structural abnormalities in an ovine model of chronic blood pressure elevation after prenatal corticosteroid exposure: implications for development of atrial fibrillation. Eur. Heart J. 27 (2006), 3045–3056.
42. Klein, L.S., Miles, W.M., Zipes, D.P., Effect of atrioventricular interval during pacing or reciprocating tachycardia on atrial size, pressure, and refractory period. Contraction-excitation feedback in human atrium. Circulation 82 (1990), 60–68.
43. Koizumi, K., Nishino, H., Brooks, C.M., Centers involved in the autonomic reflex reactions originating from stretching of the atria. Proc. Natl. Acad. Sci. U. S. A. 74 (1977), 2177–2181.
44. Konings, K.T., Kirchhof, C.J., Smeets, J.R., Wellens, H.J., Penn, O.C., Allessie, M.A., High-density mapping of electrically induced atrial fibrillation in humans. Circulation 89 (1994), 1665–1680.
45. Kuijpers, N.H., Potse, M., van Dam, P.M., ten Eikelder, H.M., Verheule, S., Prinzen, F.W., Schotten, U., Mechanoelectrical coupling enhances initiation and affects perpetuation of atrial fibrillation during acute atrial dilation. Heart Rhythm 8 (2011), 429–436.
46. Lau, D.H., Mackenzie, L., Kelly, D.J., Psaltis, P.J., Brooks, A.G., Worthington, M., Rajendram, A., Kelly, D.R., Zhang, Y., Kuklik, P., Nelson, A.J., Wong, C.X., Worthley, S.G., Rao, M., Faull, R.J., Edwards, J., Saint, D.A., Sanders, P., Hypertension and atrial fibrillation: evidence of progressive atrial remodeling with electrostructural correlate in a conscious chronically instrumented ovine model. Heart Rhythm 7 (2010), 1282–1290.
47. Lau, D.H., Mackenzie, L., Kelly, D.J., Psaltis, P.J., Worthington, M., Rajendram, A., Kelly, D.R., Nelson, A.J., Zhang, Y., Kuklik, P., Brooks, A.G., Worthley, S.G., Faull, R.J., Rao, M., Edwards, J., Saint, D.A., Sanders, P., Short-term hypertension is associated with the development of atrial fibrillation substrate: a study in an ovine hypertensive model. Heart Rhythm 7 (2010), 396–404.
48. Lau, D.H., Psaltis, P.J., Mackenzie, L., Kelly, D.J., Carbone, A., Worthington, M., Nelson, A.J., Zhang, Y., Kuklik, P., Wong, C.X., Edwards, J., Saint, D.A., Worthley, S.G., Sanders, P., Atrial remodeling in an ovine model of anthracycline-induced nonischemic cardiomyopathy: remodeling of the same sort. J. Cardiovasc. Electrophysiol. 22 (2011), 175–182.
49. Lau, D.H., Schotten, U., Mahajan, R., Antic, N.A., Hatem, S.N., Pathak, R.K., Hendriks, J.M., Kalman, J.M., Sanders, P., Novel mechanisms in the pathogenesis of atrial fibrillation: practical applications. Eur. Heart J. 37 (2016), 1573–1581.
50. Lau, D.H., Shipp, N.J., Kelly, D.J., Thanigaimani, S., Neo, M., Kuklik, P., Lim, H.S., Zhang, Y., Drury, K., Wong, C.X., Chia, N.H., Brooks, A.G., Dimitri, H., Saint, D.A., Brown, L., Sanders, P., Atrial arrhythmia in ageing spontaneously hypertensive rats: unraveling the substrate in hypertension and ageing. PLoS One, 8, 2013, e72416.
51. Li, D., Fareh, S., Leung, T.K., Nattel, S., Promotion of atrial fibrillation by heart failure in dogs: atrial remodeling of a different sort. Circulation 100 (1999), 87–95.
52. Li, D., Shinagawa, K., Pang, L., Leung, T.K., Cardin, S., Wang, Z., Nattel, S., Effects of angiotensin-converting enzyme inhibition on the development of the atrial fibrillation substrate in dogs with ventricular tachypacing-induced congestive heart failure. Circulation 104 (2001), 2608–2614.
53. Li, D., Shinagawa, K., Pang, L., Leung, T.K., Cardin, S., Wang, Z., Nattel, S., Effects of angiotensin-converting enzyme inhibition on the development of the atrial fibrillation substrate in dogs with ventricular tachypacing–induced congestive heart failure. Circulation 104 (2001), 2608–2614.
54. Linz, D., Hohl, M., Ukena, C., Mahfoud, F., Wirth, K., Neuberger, H.R., Bohm, M., Obstructive respiratory events and premature atrial contractions after cardioversion. Eur. Respir. J. 45 (2015), 1332–1340.
55. Linz, D., Linz, B., Hohl, M., Bohm, M., Atrial arrhythmogenesis in obstructive sleep apnea: therapeutic implications. Sleep. Med. Rev. 26 (2016), 87–94.
56. Linz, D., Schotten, U., Neuberger, H.-R., Böhm, M., Wirth, K., Negative tracheal pressure during obstructive respiratory events promotes atrial fibrillation by vagal activation. Heart Rhythm 8 (2011), 1436–1443.
57. Linz, D., Ukena, C., Mahfoud, F., Neuberger, H.R., Bohm, M., Atrial autonomic innervation: a target for interventional antiarrhythmic therapy?. J. Am. Coll. Cardiol. 63 (2014), 215–224.
58. Liu, L., Nattel, S., Differing sympathetic and vagal effects on atrial fibrillation in dogs: role of refractoriness heterogeneity. Am. J. Physiol. 273 (1997), H805–H816.
59. Mahajan, R., Lau, D.H., Brooks, A.G., Shipp, N.J., Manavis, J., Wood, J.P., Finnie, J.W., Samuel, C.S., Royce, S.G., Twomey, D.J., Thanigaimani, S., Kalman, J.M., Sanders, P., Electrophysiological, electroanatomical, and structural remodeling of the atria as consequences of sustained obesity. J. Am. Coll. Cardiol. 66 (2015), 1–11.
60. Malcolme-Lawes, L.C., Juli, C., Karim, R., Bai, W., Quest, R., Lim, P.B., Jamil-Copley, S., Kojodjojo, P., Ariff, B., Davies, D.W., Rueckert, D., Francis, D.P., Hunter, R., Jones, D., Boubertakh, R., Petersen, S.E., Schilling, R., Kanagaratnam, P., Peters, N.S., Automated analysis of atrial late gadolinium enhancement imaging that correlates with endocardial voltage and clinical outcomes: a 2-center study. Heart Rhythm 10 (2013), 1184–1191.
61. Malmo, V., Nes, B.M., Amundsen, B.H., Tjonna, A.E., Stoylen, A., Rossvoll, O., Wisloff, U., Loennechen, J.P., Aerobic interval training reduces the burden of atrial fibrillation in the short term: a randomized trial. Circulation 133 (2016), 466–473.
62. Medi, C., Kalman, J.M., Spence, S.J., Teh, A.W., Lee, G., Bader, I., Kaye, D.M., Kistler, P.M., Atrial electrical and structural changes associated with longstanding hypertension in humans: implications for the substrate for atrial fibrillation. J. Cardiovasc. Electrophysiol. 22 (2011), 1317–1324.
63. Milberg, P., Frommeyer, G., Ghezelbash, S., Rajamani, S., Osada, N., Razvan, R., Belardinelli, L., Breithardt, G., Eckardt, L., Sodium channel block by ranolazine in an experimental model of stretch-related atrial fibrillation: prolongation of interatrial conduction time and increase in post-repolarization refractoriness. Europace 15 (2013), 761–769.
64. Morton, J.B., Sanders, P., Vohra, J.K., Sparks, P.B., Morgan, J.G., Spence, S.J., Grigg, L.E., Kalman, J.M., Effect of chronic right atrial stretch on atrial electrical remodeling in patients with an atrial septal defect. Circulation 107 (2003), 1775–1782.
65. Munger, T.M., Dong, Y.X., Masaki, M., Oh, J.K., Mankad, S.V., Borlaug, B.A., Asirvatham, S.J., Shen, W.K., Lee, H.C., Bielinski, S.J., Hodge, D.O., Herges, R.M., Buescher, T.L., Wu, J.H., Ma, C., Zhang, Y., Chen, P.S., Packer, D.L., Cha, Y.M., Electrophysiological and hemodynamic characteristics associated with obesity in patients with atrial fibrillation. J. Am. Coll. Cardiol. 60 (2012), 851–860.
66. Naruse, Y., Tada, H., Satoh, M., Yanagihara, M., Tsuneoka, H., Hirata, Y., Ito, Y., Kuroki, K., Machino, T., Yamasaki, H., Igarashi, M., Sekiguchi, Y., Sato, A., Aonuma, K., Concomitant obstructive sleep apnea increases the recurrence of atrial fibrillation following radiofrequency catheter ablation of atrial fibrillation: clinical impact of continuous positive airway pressure therapy. Heart Rhythm 10 (2013), 331–337.
67. Nazir, S.A., Lab, M.J., Mechanoelectric feedback in the atrium of the isolated Guinea-pig heart. Cardiovasc. Res. 32 (1996), 112–119.
68. Neuberger, H.-R., Schotten, U., Verheule, S., Eijsbouts, S., Blaauw, Y., van Hunnik, A., Allessie, M., Development of a substrate of atrial fibrillation during chronic atrioventricular block in the goat. Circulation 111 (2005), 30–37.
69. Ng, C.Y., Liu, T., Shehata, M., Stevens, S., Chugh, S.S., Wang, X., Meta-analysis of obstructive sleep apnea as predictor of atrial fibrillation recurrence after catheter ablation. Am. J. Cardiol. 108 (2011), 47–51.
70. Pathak, R.K., Elliott, A., Middeldorp, M.E., Meredith, M., Mehta, A.B., Mahajan, R., Hendriks, J.M., Twomey, D., Kalman, J.M., Abhayaratna, W.P., Lau, D.H., Sanders, P., Impact of CARDIO respiratory FITness on arrhythmia recurrence in obese individuals with atrial fibrillation: the CARDIO-FIT study. J. Am. Coll. Cardiol. 66 (2015), 985–996.
71. Pathak, R.K., Middeldorp, M.E., Lau, D.H., Mehta, A.B., Mahajan, R., Twomey, D., Alasady, M., Hanley, L., Antic, N.A., McEvoy, R.D., Kalman, J.M., Abhayaratna, W.P., Sanders, P., Aggressive risk factor reduction study for atrial fibrillation and implications for the outcome of ablation: the ARREST-AF cohort study. J. Am. Coll. Cardiol. 64 (2014), 2222–2231.
72. Pathak, R.K., Middeldorp, M.E., Meredith, M., Mehta, A.B., Mahajan, R., Wong, C.X., Twomey, D., Elliott, A.D., Kalman, J.M., Abhayaratna, W.P., Lau, D.H., Sanders, P., Long-term effect of goal-directed weight management in an atrial fibrillation cohort: a long-term follow-up study (LEGACY). J. Am. Coll. Cardiol. 65 (2015), 2159–2169.
73. Peyronnet, R., Nerbonne, J.M., Kohl, P., Cardiac mechano-gated ion channels and arrhythmias. Circ. Res. 118 (2016), 311–329.
74. Polontchouk, L., Haefliger, J.-A., Ebelt, B., Schaefer, T., Stuhlmann, D., Mehlhorn, U., Kuhn-Regnier, F., De Vivie, E.R., Dhein, S., Effects of chronic atrial fibrillation on gap junction distribution in human and rat atria. J. Am. Coll. Cardiol. 38 (2001), 883–891.
75. Ravelli, F., Allessie, M., Effects of atrial dilatation on refractory period and vulnerability to atrial fibrillation in the isolated Langendorff-perfused rabbit heart. Circulation 96 (1997), 1686–1695.
76. Ravelli, F., Mase, M., del Greco, M., Marini, M., Disertori, M., Acute atrial dilatation slows conduction and increases AF vulnerability in the human atrium. J. Cardiovasc. Electrophysiol. 22 (2011), 394–401.
77. Roberts-Thomson, K.C., John, B., Worthley, S.G., Brooks, A.G., Stiles, M.K., Lau, D.H., Kuklik, P., Shipp, N.J., Kalman, J.M., Sanders, P., Left atrial remodeling in patients with atrial septal defects. Heart Rhythm 6 (2009), 1000–1006.
78. Roberts-Thomson, K.C., Stevenson, I., Kistler, P.M., Haqqani, H.M., Spence, S.J., Goldblatt, J.C., Sanders, P., Kalman, J.M., The role of chronic atrial stretch and atrial fibrillation on posterior left atrial wall conduction. Heart Rhythm 6 (2009), 1109–1117.
79. Rucker-Martin, C., Milliez, P., Tan, S., Decrouy, X., Recouvreur, M., Vranckx, R., Delcayre, C., Renaud, J.-F., Dunia, I., Segretain, D., Hatem, S.N., Chronic hemodynamic overload of the atria is an important factor for gap junction remodeling in human and rat hearts. Cardiovasc. Res. 72 (2006), 69–79.
80. Rudolph, T.K., Ravekes, T., Klinke, A., Friedrichs, K., Mollenhauer, M., Pekarova, M., Ambrozova, G., Martiskova, H., Kaur, J.J., Matthes, B., Schwoerer, A., Woodcock, S.R., Kubala, L., Freeman, B.A., Baldus, S., Rudolph, V., Nitrated fatty acids suppress angiotensin II-mediated fibrotic remodelling and atrial fibrillation. Cardiovasc. Res. 109 (2016), 174–184.
81. Sanders, P., Morton, J.B., Davidson, N.C., Spence, S.J., Vohra, J.K., Sparks, P.B., Kalman, J.M., Electrical remodeling of the atria in congestive heart failure: electrophysiological and electroanatomic mapping in humans. Circulation 108 (2003), 1461–1468.
82. Satoh, T., Zipes, D.P., Unequal atrial stretch in dogs increases dispersion of refractoriness conducive to developing atrial fibrillation. J. Cardiovasc. Electrophysiol. 7 (1996), 833–842.
83. Savelieva, I., Kakouros, N., Kourliouros, A., Camm, A.J., Upstream therapies for management of atrial fibrillation: review of clinical evidence and implications for European Society of Cardiology guidelines. Part I: primary prevention. Europace 13 (2011), 308–328.
84. Savelieva, I., Kakouros, N., Kourliouros, A., Camm, A.J., Upstream therapies for management of atrial fibrillation: review of clinical evidence and implications for European Society of Cardiology guidelines. Part II: secondary prevention. Europace 13 (2011), 610–625.
85. Schotten, U., Verheule, S., Kirchhof, P., Goette, A., Pathophysiological mechanisms of atrial fibrillation: a translational appraisal. Physiol. Rev. 91 (2011), 265–325.
86. Seo, K., Inagaki, M., Nishimura, S., Hidaka, I., Sugimachi, M., Hisada, T., Sugiura, S., Structural heterogeneity in the ventricular wall plays a significant role in the initiation of stretch-induced arrhythmias in perfused rabbit right ventricular tissues and whole heart preparations. Circ. Res. 106 (2010), 176–184.
87. Sideris, D.A., Toumanidis, S.T., Thodorakis, M., Kostopoulos, K., Tselepatiotis, E., Langoura, C., Stringli, T., Moulopoulos, S.D., Some observations on the mechanism of pressure related atrial fibrillation. Eur. Heart J. 15 (1994), 1585–1589.
88. Solti, F., Vecsey, T., Kekesi, V., Juhasz-Nagy, A., The effect of atrial dilatation on the genesis of atrial arrhythmias. Cardiovasc. Res. 23 (1989), 882–886.
89. Sosunov, E.A., Anyukhovsky, E.P., Rosen, M.R., Adrenergic-cholinergic interaction that modulates repolarization in the atrium is altered with aging. J. Cardiovasc. Electrophysiol. 13 (2002), 374–379.
90. Sparks, P.B., Mond, H.G., Vohra, J.K., Jayaprakash, S., Kalman, J.M., Electrical remodeling of the atria following loss of atrioventricular synchrony: a long-term study in humans. Circulation 100 (1999), 1894–1900.
91. Sparks, P.B., Mond, H.G., Vohra, J.K., Yapanis, A.G., Grigg, L.E., Kalman, J.M., Mechanical remodeling of the left atrium after loss of atrioventricular synchrony. A long-term study in humans. Circulation 100 (1999), 1714–1721.
92. Stevenson, I.H., Teichtahl, H., Cunnington, D., Ciavarella, S., Gordon, I., Kalman, J.M., Prevalence of sleep disordered breathing in paroxysmal and persistent atrial fibrillation patients with normal left ventricular function. Eur. Heart J. 29 (2008), 1662–1669.
93. Takeuchi, S., Akita, T., Takagishi, Y., Watanabe, E., Sasano, C., Honjo, H., Kodama, I., Disorganization of gap junction distribution in dilated atria of patients with chronic atrial fibrillation. Circ. J. 70 (2006), 575–582.
94. Teh, A.W., Kistler, P.M., Lee, G., Medi, C., Heck, P.M., Spence, S.J., Morton, J.B., Sanders, P., Kalman, J.M., Long-term effects of catheter ablation for lone atrial fibrillation: progressive atrial electroanatomic substrate remodeling despite successful ablation. Heart Rhythm 9 (2012), 473–480.
95. Tse, H.F., Pelosi, F., Oral, H., Knight, B.P., Strickberger, S.A., Morady, F., Effects of simultaneous atrioventricular pacing on atrial refractoriness and atrial fibrillation inducibility: role of atrial mechanoelectrical feedback. J. Cardiovasc Electrophysiol. 12 (2001), 43–50.
96. Vaziri, S.M., Larson, M.G., Benjamin, E.J., Levy, D., Echocardiographic predictors of nonrheumatic atrial fibrillation. The Framingham heart study. Circulation 89 (1994), 724–730.
97. Verheule, S., Tuyls, E., Gharaviri, A., Hulsmans, S., van Hunnik, A., Kuiper, M., Serroyen, J., Zeemering, S., Kuijpers, N.H.L., Schotten, U., Loss of continuity in the thin epicardial layer because of endomysial fibrosis increases the complexity of atrial fibrillatory conduction. Circ. Arrhythm. Electrophysiol. 6 (2013), 202–211.
98. Verheule, S., Wilson, E., Banthia, S., Everett, T.H.t., Shanbhag, S., Sih, H.J., Olgin, J., Direction-dependent conduction abnormalities in a canine model of atrial fibrillation due to chronic atrial dilatation. Am. J. Physiol. Heart Circ. Physiol. 287 (2004), H634–H644.
99. Verheule, S., Wilson, E., Everett, T.t., Shanbhag, S., Golden, C., Olgin, J., Alterations in atrial electrophysiology and tissue structure in a canine model of chronic atrial dilatation due to mitral regurgitation. Circulation 107 (2003), 2615–2622.
100. Verkerk, A.O., Geuzebroek, G.S., Veldkamp, M.W., Wilders, R., Effects of acetylcholine and noradrenalin on action potentials of isolated rabbit sinoatrial and atrial myocytes. Front. Physiol., 3, 2012, 174.
101. Walters, T.E., Lee, G., Spence, S., Larobina, M., Atkinson, V., Antippa, P., Goldblatt, J., O'Keefe, M., Sanders, P., Kistler, P.M., Kalman, J.M., Acute atrial stretch results in conduction slowing and complex signals at the pulmonary vein to left atrial junction: insights into the mechanism of pulmonary vein arrhythmogenesis. Circ. Arrhythm. Electrophysiol. 7 (2014), 1189–1197.
102. Wijffels, M.C., Kirchhof, C.J., Dorland, R., Allessie, M.A., Atrial fibrillation begets atrial fibrillation. A study in awake chronically instrumented goats. Circulation 92 (1995), 1954–1968.
103. Wijffels, M.C.E.F., Kirchhof, C.J.H.J., Dorland, R., Power, J., Allessie, M.A., Electrical remodeling due to atrial fibrillation in chronically instrumented conscious goats: roles of neurohumoral changes, ischemia, atrial stretch, and high rate of electrical activation. Circulation 96 (1997), 3710–3720.
104. Wong, C.X., John, B., Brooks, A.G., Chandy, S.T., Kuklik, P., Lau, D.H., Sullivan, T., Roberts-Thomson, K.C., Sanders, P., Direction-dependent conduction abnormalities in the chronically stretched atria. Europace 14 (2012), 954–961.
105. Wong, C.X., Sullivan, T., Sun, M.T., Mahajan, R., Pathak, R.K., Middeldorp, M., Twomey, D., Ganesan, A.N., Rangnekar, G., Roberts-Thomson, K.C., Lau, D.H., Sanders, P., Obesity and the risk of incident, post-operative, and post-ablation atrial fibrillation. JACC Clin. Electrophysiol. 1 (2015), 139–152.
106. Yamazaki, M., Filgueiras-Rama, D., Berenfeld, O., Kalifa, J., Ectopic and reentrant activation patterns in the posterior left atrium during stretch-related atrial fibrillation. Prog. Biophys. Mol. Biol. 110 (2012), 269–277.
107. Yamazaki, M., Vaquero, L.M., Hou, L., Campbell, K., Zlochiver, S., Klos, M., Mironov, S., Berenfeld, O., Honjo, H., Kodama, I., Jalife, J., Kalifa, J., Mechanisms of stretch-induced atrial fibrillation in the presence and the absence of adrenocholinergic stimulation: interplay between rotors and focal discharges. Heart Rhythm 6 (2009), 1009–1017.
108. Zipes, D.P., Mihalick, M.J., Robbins, G.T., Effects of selective vagal and stellate ganglion stimulation of atrial refractoriness. Cardiovasc Res. 8 (1974), 647–655.