Atrial fibrillation driven by micro-anatomic intramural re-entry revealed by simultaneous sub-epicardial and sub-endocardial optical mapping in explanted human hearts

European Heart Journal

Volumn 36, Issue 35, 2015, Pages 2390-2401

  Hansen, Brian J ^a   Zhao, Jichao ^b   Csepe, Thomas A ^a   Moore, Brandon T ^a   Li, Ning ^a   Jayne, Laura A ^a   Kalyanasundaram, Anuradha ^a   Lim, Praise ^b   Bratasz, Anna ^a,d   Powell, Kimerly A ^a,c,d   Simonetti, Orlando P ^a,d   Higgins, Robert S D ^a,d   Kilic, Ahmet ^a,d   Mohler, Peter J ^a,d   Janssen, Paul M L ^a,d   Weiss, Raul ^a,d   Hummel, John D ^a,d   Fedorov, Vadim V ^a,d  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

Atrial fibrillation; Catheter radiofrequency ablation; Fibrosis; Gadolinium enhanced MRI; Intramural re entry; Optical mapping; Rotor

Indexed keywords

GADOLINIUM; PINACIDIL; CONTRAST MEDIUM;

ARTICLE; ATRIAL FIBRILLATION; CARDIOVASCULAR CATHETER; CARDIOVASCULAR MAGNETIC RESONANCE; CARDIOVASCULAR SYSTEM EXAMINATION; CYTOARCHITECTURE; EX VIVO STUDY; EXPLANT; FIBROSING ALVEOLITIS; HEART ATRIUM PACING; HEART EXPLANT; HEART FUNCTION; HEART MUSCLE REFRACTORY PERIOD; HISTOLOGY; HUMAN; HUMAN TISSUE; PRIORITY JOURNAL; RADIOFREQUENCY ABLATION; REENTRY ARRHYTHMIA; SUB ENDOCARDIAL OPTICAL MAPPING; SUB EPICARDIAL OPTICAL MAPPING; THREE DIMENSIONAL IMAGING; ADULT; AGED; CARDIAC IMAGING; EPICARDIUM MAPPING; HEART ATRIUM; MAGNETIC RESONANCE ANGIOGRAPHY; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES;

ADULT; AGED; ATRIAL FIBRILLATION; CARDIAC IMAGING TECHNIQUES; CONTRAST MEDIA; EPICARDIAL MAPPING; GADOLINIUM; HEART ATRIA; HUMANS; MAGNETIC RESONANCE ANGIOGRAPHY; MIDDLE AGED;

EID: 84929341595     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehv233     Document Type: Article

References (38)

1. Nishida K, Nattel S. Atrial fibrillation compendium: historical context and detailed translational perspective on an important clinical problem. Circ Res 2014;114: 1447-1452.
2. Mahnkopf C, Badger TJ, Burgon NS, Daccarett M, Haslam TS, Badger CT, McGann CJ, Akoum N, Kholmovski E, MacLeod RS, Marrouche NF. Evaluation of the left atrial substrate in patients with lone atrial fibrillation using delayedenhanced MRI: implications for disease progression and response to catheter ablation. Heart Rhythm 2010;7:1475-1481.
3. Burstein B, Nattel S. Atrial fibrosis: mechanisms and clinical relevance in atrial fibrillation. J Am Coll Cardiol 2008;51:802-809.
4. de Groot NM, Houben RP, Smeets JL, Boersma E, Schotten U, Schalij MJ, Crijns H, Allessie MA. Electropathological substrate of longstanding persistent atrial fibrillation in patients with structural heart disease: epicardial breakthrough. Circulation 2010;122:1674-1682.
5. Allessie MA, de Groot NM, Houben RP, Schotten U, Boersma E, Smeets JL, Crijns HJ. Electropathological substrate of long-standing persistent atrial fibrillation in patients with structural heart disease: longitudinal dissociation. Circ Arrhythm Electrophysiol 2010;3:606-615.
6. Zhao J, Butters TD, Zhang H, Pullan AJ, LeGrice IJ, Sands GB, Smaill BH. An imagebased model of atrial muscular architecture: effects of structural anisotropy on electrical activation. Circ Arrhythm Electrophysiol 2012;5:361-370.
7. Shivkumar K, Ellenbogen KA, Hummel JD, Miller JM, Steinberg JS. Acute termination of human atrial fibrillation by identification and catheter ablation of localized rotors and sources: first multicenter experience of focal impulse and rotor modulation (FIRM) ablation. J Cardiovasc Electrophysiol 2012;23:1277-1285.
8. Haissaguerre M, Hocini M, Denis A, Shah AJ, Komatsu Y, Yamashita S, Daly M, Amraoui S, Zellerhoff S, Picat MQ, Quotb A, Jesel L, Lim H, Ploux S, Bordachar P, Attuel G, Meillet V, Ritter P, Derval N, Sacher F, Bernus O, Cochet H, Jais P, Dubois R. Driver domains in persistent atrial fibrillation. Circulation 2014;130:530-538.
9. Lee G, Kumar S, Teh A, Madry A, Spence S, Larobina M, Goldblatt J, Brown R, Atkinson V, Moten S, Morton JB, Sanders P, Kistler PM, Kalman JM. Epicardial wave mapping in human long-lasting persistent atrial fibrillation: transient rotational circuits, complex wavefronts, and disorganized activity. Eur Heart J 2014;35:86-97.
10. Narayan SM, Krummen DE, Clopton P, Shivkumar K, Miller JM. Direct or coincidental elimination of stable rotors or focal sources may explain successful atrial fibrillation ablation: on-treatment analysis of the CONFIRM trial (Conventional ablation for AF with or without focal impulse and rotor modulation). J Am Coll Cardiol 2013; 62:138-147.
11. Allessie M, de GN. Rotors during AF: drivers or bystanders? Eur Heart J 2014;35: 63-65.
12. Cochet H, Scherr D, Zellerhoff S, Sacher F, Derval N, Denis A, Knecht S, Komatsu Y, Montaudon M, Laurent F, Pieske BM, Hocini M, Haissaguerre M, Jais P. Atrial structure and function 5 years after successful ablation for persistent atrial fibrillation: an MRI study. J Cardiovasc Electrophysiol 2014;25:671-679.
13. Wyse DG, Van Gelder IC, Ellinor PT, Go AS, Kalman JM, Narayan SM, Nattel S, Schotten U, Rienstra M. Lone atrial fibrillation: does it exist? J Am Coll Cardiol 2014;63:1715-1723.
14. Fedorov VV, Glukhov AV, Ambrosi CM, Kostecki G, Chang R, Janks D, Schuessler RB, Moazami N, Nichols CG, Efimov IR. Effects of KATP channel openers diazoxide and pinacidil in coronary-perfused atria and ventricles from failing and non-failing human hearts. J Mol Cell Cardiol 2011;51:215-225.
15. Fedorov VV, Glukhov AV, Chang R, Kostecki G, Aferol H, Hucker WJ, Wuskell JP, Loew LM, Schuessler RB, Moazami N, Efimov IR. Optical mapping of the isolated coronary-perfused human sinus node. J Am Coll Cardiol 2010;56:1386-1394.
16. Sanders P, Morton JB, Davidson NC, Spence SJ, Vohra JK, Sparks PB, Kalman JM. Electrical remodeling of the atria in congestive heart failure: electrophysiological and electroanatomic mapping in humans. Circulation 2003;108:1461-1468.
17. Franz MR, Karasik PL, Li C, Moubarak J, Chavez M. Electrical remodeling of the human atrium: similar effects in patients with chronic atrial fibrillation and atrial flutter. J Am Coll Cardiol 1997;30:1785-1792.
18. Lou Q, Hansen BJ, Fedorenko O, Csepe T, Kalyanasundaram A, Li N, Hage L, Glukhov AV, Billman GE, Weiss R, Mohler PJ, Gyorke S, Biesiadecki BJ, Carnes C, Fedorov VV. Upregulation of adenosine A1 receptors facilitates sinoatrial node dysfunction in chronic canine heart failure by exacerbating nodal conduction abnormalities revealed by novel dual-sided intramural optical mapping. Circulation 2014;130:315-324.
19. Baxter WT, Mironov SF, Zaitsev AV, Jalife J, Pertsov AM. Visualizing excitation waves inside cardiac muscle using transillumination. Biophys J 2001;80:516-530.
20. Sanders P, Berenfeld O, Hocini M, Jais P, Vaidyanathan R, Hsu LF, Garrigue S, Takahashi Y, Rotter M, Sacher F, Scavee C, Ploutz-Snyder R, Jalife J, Haissaguerre M. Spectral analysis identifies sites of high-frequency activity maintaining atrial fibrillation in humans. Circulation 2005;112:789-797.
21. Guillem MS, Climent AM, Millet J, Arenal A, Fernandez-Aviles F, Jalife J, Atienza F, Berenfeld O. Noninvasive localization of maximal frequency sites of atrial fibrillation by body surface potential mapping. Circ Arrhythm Electrophysiol 2013;6: 294-301.
22. Marrouche NF, Wilber D, Hindricks G, Jais P, Akoum N, Marchlinski F, Kholmovski E, Burgon N, Hu N, Mont L, Deneke T, Duytschaever M, Neumann T, Mansour M, Mahnkopf C, Herweg B, Daoud E, Wissner E, Bansmann P, Brachmann J. Association of atrial tissue fibrosis identified by delayed enhancement MRI and atrial fibrillation catheter ablation: the DECAAF study. JAMA 2014;311:498-506.
23. Loukas M, Tubbs RS, Tongson JM, Polepalli S, Curry B, Jordan R, Wagner T. The clinical anatomy of the crista terminalis, pectinate muscles and the teniae sagittalis. Ann Anat 2008;190:81-87.
24. Gray RA, Pertsov AM, Jalife J. Incomplete reentry and epicardial breakthrough patterns during atrial fibrillation in the sheep heart. Circulation 1996;94:2649-2661.
25. O'Neill MD, Jais P, Takahashi Y, Jonsson A, Sacher F, Hocini M, Sanders P, Rostock T, Rotter M, Pernat A, Clementy J, Haissaguerre M. The stepwise ablation approach for chronic atrial fibrillation-evidence for a cumulative effect. J Interv Card Electrophysiol 2006;16:153-167.
26. Garrey WE. Auricular fibrillation. Physiol Rev 1924;4:215-250.
27. Lewis T, Drury AN, Iliescu CC. Further observations upon the state of rapid reexcitation of the auricles. Heart 1921;8:311-340.
28. Schuessler RB, Grayson TM, Bromberg BI, Cox JL, Boineau JP. Cholinergically mediated tachyarrhythmias induced by a single extrastimulus in the isolated canine right atrium. Circ Res 1992;71:1254-1267.
29. Jalife J, Berenfeld O, Mansour M. Mother rotors and fibrillatory conduction: a mechanism of atrial fibrillation. Cardiovasc Res 2002;54:204-216.
30. Cox JL, Canavan TE, Schuessler RB, Cain ME, Lindsay BD, Stone C, Smith PK, Corr PB, Boineau JP. 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 1991;101:406-426.
31. Haissaguerre M, Hocini M, Sanders P, Takahashi Y, Rotter M, Sacher F, Rostock T, Hsu LF, Jonsson A, O'Neill MD, Bordachar P, Reuter S, Roudaut R, Clementy J, Jais P. Localized sources maintaining atrial fibrillation organized by prior ablation. Circulation 2006;113:616-625.
32. Zaitsev AV, Rozenshtraukh LV, Fast VG, Bobrovskii RV, Pertsov AM. Study of spontaneous acetylcholine-dependent tachyarrhythmias using isolated specimens of the right canine atrium by bilateral mapping of the spread of excitation. Kardiologiia 1989;29:80-85.
33. Schuessler RB, Kawamoto T, Hand DE, Mitsuno M, Bromberg BI, Cox JL, Boineau JP. Simultaneous epicardial and endocardial activation sequence mapping in the isolated canine right atrium. Circulation 1993;88:250-263.
34. Eckstein J, Maesen B, Linz D, Zeemering S, van HA, Verheule S, Allessie M, Schotten U. Time course and mechanisms of endo-epicardial electrical dissociation during atrial fibrillation in the goat. Cardiovasc Res 2011;89:816-824.
35. Yamazaki M, Mironov S, Taravant C, Brec J, Vaquero LM, Bandaru K, Avula UM, Honjo H, Kodama I, Berenfeld O, Kalifa J. Heterogeneous atrial wall thickness and stretch promote scroll waves anchoring during atrial fibrillation. Cardiovasc Res 2012;94:48-57.
36. Corradi D, Callegari S, Manotti L, Ferrara D, Goldoni M, Alinovi R, Pinelli S, Mozzoni P, Andreoli R, Asimaki A, Pozzoli A, Becchi G, Mutti A, Benussi S, Saffitz JE, Alfieri O. Persistent lone atrial fibrillation: clinicopathologic study of 19 cases. Heart Rhythm 2014;11:1250-1258.
37. Mewton N, Liu CY, Croisille P, Bluemke D, Lima JA. Assessment of myocardial fibrosis with cardiovascular magnetic resonance. J Am Coll Cardiol 2011;57:891-903.
38. Voigt N, Trausch A, Knaut M, Matschke K, Varro A, Van Wagoner DR, Nattel S, Ravens U, Dobrev D. Left-to-right atrial inward rectifier potassium current gradients in patients with paroxysmal versus chronic atrial fibrillation. Circ Arrhythm Electrophysiol 2010;3:472-480.