Radiofrequency and Cryoablation of Atrial Fibrillation in Patients Undergoing Valvular Operations Mien-Cheng Chen, MD, G. Bih-Fang Guo, MD, PhD, Jen-Ping Chang, MD, Kuo-Ho Yeh, MD, and Morgan Fu, MD Section of Cardiology, Department of Medicine, and Section of Cardiovascular Surgery, Department of Surgery, Chang Gung Memorial Hospital, Kaohsiung, Taiwan, Republic of China
Background. Previous studies have shown that the maze operation can restore sinus rhythm and atrial transport function in patients with chronic atrial fibrillation. The purpose of this study was to test the feasibility of the application of radiofrequency and cryoablation as an alternative to the classic maze operation. Methods. Twelve patients undergoing mitral valve procedures were included in this study. Radiofrequency and cryoablation were applied to create lesions in both atria to simulate the classic maze operation. Results. There were two surgical deaths. At the mean follow-up of 10.25 months for the remaining 10 patients; 6 were in sinus rhythm, 2 in atrial rhythm, 1 in paroxys-
mal atrial tachycardia, and 1 in atrial fibrillation. Doppler echocardiography at 6-month follow-up showed emergence of biatrial transport function in 3 patients and right atrial contractility in 8. At 12-month follow-up of 5 patients, Doppler echocardiography showed biatrial transport function in 3 and right atrial contractility in 4. Conclusions. Our modified maze procedure during valvular operation is effective for achieving an acceptable success rate to restore sinus rhythm and atrial transport function in patients with chronic atrial fibrillation.
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transport function in patients with chronic AF undergoing valvular operations. This combination may be advantageous because the atrial linear lesions created by radiofrequency energy may obviate the need for extensive atrial incision in the original maze surgical procedure and, therefore, minimize exsanguination and reduce myocardial ischemic time.
trial fibrillation (AF) is the most common sustained cardiac arrhythmia and incurs significant morbidity and mortality as a result of the risk of systemic embolization [1, 2] and compromised cardiac function [3]. Despite a wide range of selection of antiarrhythmic drugs [4, 5], as well as availability of electric cardioversion [6, 7], the management of AF remains unsatisfactory as recurrence and proarrhythmia are common. Control of the ventricular rate response to improve cardiac function through the modification of atrioventricular junction by radiofrequency energy has recently been adopted [3, 8]. However, AF persists. The maze surgical procedure involving incisions of both atria, initially described by Cox and colleagues [9 –12], has offered a curative treatment of AF as this method is highly successful in the restoration of sinus rhythm and atrial transport function in patients with lone AF as well as in patients with organic heart diseases [13, 14]. However, the combination of surgical procedures imposes on patients extensive atrial incision, suturing, and greater blood loss as well as longer cardiac arrest [14]. The purpose of the present study was to determine whether the combination of radiofrequency catheter ablation and cryoablation to simulate the maze procedure was feasible to restore sinus rhythm and atrial
Accepted for publication Jan 30, 1998. Address reprint requests to Dr Chen, Section of Cardiology, Chang Gung Memorial Hospital, 123, Ta Pei Rd, Niao Sung Hsiang, Kaohsiung Hsien 83305, Taiwan, Republic of China.
© 1998 by The Society of Thoracic Surgeons Published by Elsevier Science Inc
(Ann Thorac Surg 1998;65:1666 –72) © 1998 by The Society of Thoracic Surgeons
Material and Methods Patient Population Between December 1995 and August 1996, 12 patients (9 men and 3 women, aged 32 to 76 years with mean 6 standard deviation of 50 6 14 years) underwent the modified maze procedure and simultaneous valvular operation. The clinical characteristics and procedures for each patient are summarized in Table 1. Ten patients were in New York Heart Association functional class III and 2 in class IV. All patients had spontaneously sustained AF with a mean duration of 31.3 6 30.7 months (1 to 84 months) documented by electrocardiograms. Preoperative left atrial dimension ranged from 48 to 70 mm (55.0 6 6.3 mm). These patients were not good candidates for antiarrhythmic drugs because of a history of congestive heart failure [5] and large left atrial size. All patients had mitral valve disease with concomitant aortic valve disease in 5, tricuspid valve disease in 3, and coronary artery disease in 1 patient. Informed consent was obtained from each patient. No patients were receiving any 0003-4975/98/$19.00 PII S0003-4975(98)00230-6
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Table 1. Characteristics of Patients and Outcome Patient No. 1 2 3 4 5 6 7 8 9 10 11 12
Age (y)
Sex
56 32 47 35 63 54 34 38 44 57 76 61
M M F F M F M M M M M M
NYHA
AF Duration (mo)
LA Size (mm)
Heart Disease
Procedures
Type of Maze
Rhythm
Mortality
III III III III IV III III III III III IV III
1 48 72 24 72 36 2 2 12 18 4 84
48 58 52 70 61 51 50 57 58 55 48 52
MSR, AR MSR MR, AR MSR, TR MR, TR MSR MSR, AR MSR, AR MR, TR MSR, AR MR, CAD MSR
MVR, AVR MVP MVR, AVR MVR, TAP MVP, TAP MVR MVR, AVR MVR, AVR MVR, TAP MVR, AVR MVP, CABG MVP
III III II II II II II II III II II II
S S AF S A S S AT A S S A
2 2 2 2 1 2 2 2 2 2 1 2
A 5 atrial; AF 5 atrial fibrillation; AR 5 aortic regurgitation; AT 5 atrial tachycardia; AVR 5 aortic valve replacement; CABG 5 coronary artery bypass grafting; CAD 5 coronary artery disease; F 5 female; LA 5 left atrium; M 5 male; MR 5 mitral regurgitation; MSR 5 mitral stenosis and regurgitation; MVP 5 mitral valve repair; MVR 5 mitral valve replacement; NYHA 5 New York Heart Association functional class; S 5 sinus; TAP 5 tricuspid annuloplasty; TR 5 tricuspid regurgitation.
class I or III antiarrhythmic agents at the time of the study.
Modified Maze Procedure The operative procedure was fundamentally the same as that initially described by Cox and associates except that radiofrequency energy and cryoablation were used to create the linear lesion pattern and the lesions in specific areas guided by direct visualization (Figs 1 and 2). A quadripolar steerable electrode catheter (Mansfield, Watertown, MA) with a 4-mm distal electrode and a 2-mm electrode spacing between the distal two electrodes was used for delivery of the radiofrequency energy (30 to 50 W, 30 seconds for each lesion). Radiofrequency ablation was performed using a radiofrequency generator (EPT1000; EP Technologies, Inc, Sunnyvale, CA), which delivered a continuous, quasi-sinusoidal, unmodulated radiofrequency output at 500 kHz from the distal electrode to a cutaneous dispersive pad attached to the posterior chest. Each application of energy was able to create a transmural lesion of about 8 mm in diameter, even at trabeculated regions, as evidenced by epicardial and endocardial discoloration. The impedance was kept between 150 to 170 ohms by constant saline irrigation, which minimized and washed away char formation. A line of lesion can be made by stepwise point energy application. The radiofrequency energy was first delivered to the epicardial surface of right atrium before the cardiopulmonary bypass, starting from the junction of the superior vena cava and the right atrium toward the inferior vena cava, 1 cm away from the sinus node but parallel to the sulcus terminalis. A second line was begun obliquely from this line toward the atrioventricular groove. A third line was made between the first line and the left atrial incision. After these epicardial lesions were finished, the right atrial appendage was excised and the cardiopulmonary bypass was commenced. The right
atrium was entered by incision on the lateral part of the right atrium from the base of the resected appendage. The remaining lesions were approached endocardially in the right atrium under partial cardiopulmonary bypass and in the left atrium after cardioplegia and the left atrial incision. We also applied radiofrequency energy to the lateral part of the isthmus between the tricuspid annulus and inferior vena cava, except for the first 3 patients. The left atrial appendage was ligated after radiofrequency energy was applied around its base. The type of maze procedure chosen depended on the course of the sinus node artery. We applied cryoablation (15 mm head probe, 260°C for 3 minutes; Frigitronics, Shelton, CT) to produce endocardial lesions at the mitral annulus over the coronary sinus, the anteroseptal and posterosuperior part of the interatrial septum, and the posterolateral part of the tricuspid annulus. These areas were either too thick or not easily accessible with the radiofrequency ablation catheter. The times for the maze procedure, cardiopulmonary bypass, and aortic cross-clamping were recorded.
Postoperative Management Daily pericardial drainage was monitored until the drainage tubes were removed. Cardiac rhythm was continuously monitored after operation until a stable rhythm returned. Both atrial and ventricular temporary pacing wires were used to pace the patient if there was postoperative sinus node dysfunction or bradycardia. Postoperative atrial fibrillation was treated with procainamide.
Electrocardiography, Doppler Echocardiography, and Medications After discharge, patients were followed monthly for adjustment of medication, evaluation of rhythm, and signs of myocardial ischemia. Early diastolic ventricular filling and filling by atrial contraction across the tricuspid and
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mitral valves were assessed by Doppler echocardiography 3, 6, and 12 months after operation. Anticoagulation with warfarin was used in all patients and discontinued only in patients when they showed atrial rhythm and documented atrial contraction after reparative operation.
Results Surgical Procedures On the basis of the course of the sinus nodal arteries, 3 patients with a superior route (patients 1, 2, 9) underwent
Fig 2. Modified maze III procedure. The ablation line connecting the superior vena cava to the incision of the left atrium is shifted downward as compared with the modified maze II procedure. (Abbreviations are as in Figure 1.)
Fig 1. Modified maze II procedure, shown in epicardial (A) and endocardial (B) views of the atria. (circle 5 cryoablation; dotted line 5 radiofrequency ablation; FO 5 fossa ovalis; IVC 5 inferior vena cava; LAA 5 left atrial appendage; MV 5 mitral valve; PV 5 pulmonary vein; RAA 5 right atrial appendage; solid line with cross bars 5 incision and suturing; SVC 5 superior vena cava; TV 5 tricuspid valve.)
modified maze III procedure. The remaining 9 patients with a lateral route underwent a modified maze II procedure. Procedures performed simultaneously with the modified maze procedures are listed in Table 1. Eight patients underwent mitral valve replacement, with concomitant aortic valve replacement in 5 and tricuspid annuloplasty in 2. The remaining 4 patients underwent mitral valve repair, with concomitant tricuspid annuloplasty in 1, and coronary bypass grafting in 1, who had left anterior descending artery disease. The modified maze procedure using radiofrequency application required 30.5 to 72 minutes (53.7 6 14.5 minutes), including the mean left atrial radiofrequency ablation time of 29.5
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Table 2. Final Results at Follow-up
Variable Electrocardiographic features Sinus Atrial Paroxysmal atrial tachycardia Atrial flutter Atrial fibrillation Doppler echocardiography A wave in transmitral flow A wave in transtricuspid flow
6-Month Follow-up (n 5 10)
12-Month Follow-up (n 5 5)
5 2 1 1 1
4 0 0 0 1
3 8
3 4
minutes (21 to 36 minutes) (ie, additional ischemic time). The aortic cross-clamp time ranged from 129 to 249 minutes (183 6 45 minutes), and the cardiopulmonary bypass time varied from 166 to 332 minutes (253 6 50 minutes). Postoperatively, the maximal daily pericardial tube drainage (blood loss), which always occurred during the first 24 hours, ranged from 250 to 550 mL (365 6 116 mL).
Morbidity and Mortality There were two in-hospital deaths. One patient (patient 5), who had a normal preoperative coronary artery angiogram, had development of an acute inferior wall myocardial infarction postoperatively and died of massive cerebral infarction on the 17th day after operation while in atrial rhythm, despite no evidence of atrial thrombus by echocardiography. The other patient (patient 11) died of acute renal failure and heart failure 1 month after operation.
Postoperative Cardiac Rhythm Immediately after operation, AF disappeared in 11 patients (92%) with 4 patients in sinus rhythm, 5 in atrial rhythm, and 2 in junctional rhythm. While recuperating in the hospital, 5 patients reverted to sinus rhythm from atrial rhythm (n 5 2), junctional rhythm (n 5 2), and AF (n 5 1). However, 1 patient went back to AF from sinus rhythm and another patient developed junctional rhythm from atrial rhythm. At 1-month follow-up, one more patient went back to AF from sinus rhythm. This patient’s AF became persistent throughout the 12-month follow-up period and was the only patient treated with procainamide. At 6-month follow-up for the remaining 10 patients, the rhythms were sinus in 5 patients (50%), atrial in 2 (20%), paroxysmal left atrial tachycardia with a cycle length of 320 ms by electrophysiologic study in 1 (who refused transseptal approach for catheter ablation), typical counter-clockwise atrial flutter in 1 (who refused electrophysiologic study), and persistent AF in 1 (see Tables 1, 2). Of the 5 patients who had 12-month followup, 4 had sinus rhythm, including the patient who had AF again during hospitalization and reverted to atrial flutter for the following 6 months before returning to sinus rhythm at 9-month follow-up (Fig 3). The remain-
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ing 1 patient had persistent AF throughout the follow-up. Because of the small number of patients, we could not specifically address the issue of correlation between success rate and age, left atrial size, or AF duration.
Postoperative Doppler Echocardiographic Study At 6-month follow-up, the transmitral atrial wave was observed in 3 of 10 patients (30%), 2 of them receiving the maze III procedure. The transtricuspid atrial wave was observed in 8 of 10 patients (80%), including the patient in paroxysmal atrial tachycardia. At 12-month follow-up, the transmitral atrial wave was observed in 3 of 5 patients and the transtricuspid atrial wave was observed in 4 of 5 patients (see Table 2). A representative example is shown in Figure 3.
Functional Class At mean follow-up of 10.25 months (6 to 14 months) for the remaining 10 patients, the functional class improved to class I (n 5 7) or II (n 5 3).
Comment Application of Radiofrequency Energy to the Maze Procedure Radiofrequency catheter ablation has been widely applied to the treatment of supraventricular and ventricular tachycardias. The application of this technique to AF is still in the experimental stage. There have been few reports of successful catheter ablation of human AF [15, 16]. These were achieved by specially designed ablation catheters, requiring very long procedure time and fluoroscopic exposure in highly selected patients. The maze procedure described by Cox has apparently remained a universally applicable and potentially curative treatment of AF. However, the surgical procedure involves extensive incision and suturing of the atria. Recent results of application of radiofrequency catheter ablation to mimic the surgical maze procedure in a canine model of AF were encouraging [17]. Our results show that the maze procedure using radiofrequency energy and cryoablation with concomitant valvular operation was feasible for achieving an acceptable success rate to restore sinus rhythm and atrial transport function.
Comparison With Previous Reports Cox and associates [11] developed the maze procedures to treat patients with a majority of lone AF and 99% of patients were free of AF. Kosakai and colleagues [18] modified Cox’s maze procedures for patients with organic heart disease and 86% of patients were free of AF and atrial flutter. We used radiofrequency catheter ablation and cryoablation with modified maze procedures to obviate the need of extensive atrial incision to patients undergoing simultaneous valvular operation. In addition, pericardial patching was not necessary in our modified maze II procedure as there was no incision in the superior vena cava. Postoperative rhythms at 6-month follow-up were 80% in sinus or atrial rhythm. Five patients
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Fig 3. Surface electrocardiograms and the atrial transtricuspid (left) and transmitral (right) flows from Doppler atrioventricular diastolic flow velocity patterns before (A) and 14 months after (B) the modified maze procedure in patient 1. Atrial fibrillation without atrial transport function were noted before operation. After operation, normal sinus rhythm and biatrial transport function were evident.
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had 12-month follow-up, and the rhythms were sinus in 4 (80%). It has been known that the atrial pacemaker complex actually encompasses an area of 2 by 5 cm centering about the sinoatrial node [19]. In our study the modified maze procedure involved at least part of the pacemaker complex. This could contribute to the sinus node dysfunction observed in 7 patients (5 in atrial rhythm and 2 in junctional rhythm) immediately after operation. Similar results were also reported by Cox [11] and Kosakai [18] and their colleagues in humans. We have tried to avoid pacemaker injury by using either a maze II or III lesion pattern depending on the course of the sinus nodal arteries. Modification of the maze procedure that avoids damage to the atrial pacemaker complex and blood supply to the sinus node may reduce procedure-related sinus node dysfunction. Feinberg and colleagues [10] demonstrated restoration of right atrial contraction in 83% and left atrial contraction in 61% of 46 patients after the maze procedure in their early experience. With a modified procedure (ie, the maze III), atrial transport functions were restored to 98% in the right and 94% in the left atria [11]. Kosakai and associates [18] reported restoration of right atrial transport in 88% and left atrial transport function in 73% with their modified maze procedure in 101 patients with organic heart disease. Thus, atrial transport function of the left atrium tends to recover less than that of the right atrium. We found a similar trend in our study. An A wave was detected in 80% for transtricuspid flow, but only in 30% of patients for transmitral flow at 6-month follow-up. At 12-month follow-up of 5 patients, 3 had biatrial and 4 had right atrial transport function. The reduced tendency of recovery of the left atrial contractile function could be attributed to more extensive lesions in the left atrium and interatrial conduction delay created by the maze procedure [11]. Reducing incidence of systemic embolism is one of the goals of restoring sinus rhythm from AF. However, in the studies by Cox [11] and Kosakai [18] and their coworkers, each had one transient ischemic attack during sinus rhythm after operation. This is conceivable because coexistence sinus rhythm and AF in a patient has been documented after the maze procedure [20] and the restoration of atrial transport function may lag behind after conversion of atrial flutter by pacing or electrical cardioversion [21]. One patient in our study died of massive cerebral infarction after mitral repair while in atrial rhythm, despite being under adequate anticoagulation with no evidence of atrial thrombus using transthoracic echocardiography. Although we could not exclude other possibilities, the cause of this patient’s death was most likely attributable to systemic embolization to the cerebral and coronary circulation, as the coronary angiogram was normal before operation. In addition, the time course was too short for it to be a result of coronary intimal hyperplasia at the site of cryoablation [22, 23]. Thus, systemic embolism can occur during the early postoperative period, although AF has been terminated. In our study, the aortic cross-clamp time and cardiopulmonary bypass time were longer than those in the
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study by Kawaguchi and colleagues [14]. This was a result of valve repair using the Carpentier technique attempted in every patient. In average, this took 100 6 20 minutes, and if failed, the mitral valve replacement was performed. However, our modified maze procedure took only 30.5 to 72 minutes (53.7 6 14.5 minutes), including the mean left atrial ablation time of 29.5 minutes (21 to 36 minutes). The latter reflects a shorter ischemic time as compared with that in the series by Kosakai and associates [22]. With further refinement of the ablation catheter, the procedure time could be shortened and the risk of combining the maze procedure with valvular operation should be further reduced. Blood loss was less in our study than in the study by Kawaguchi and colleagues [14] (365 6 116 mL versus 1014 6 513 mL). This could be attributed to less incision in our modified method. Thus, homeostasis may not be a critical problem using our modified maze procedure, even combined with valvular operation. This should be another impact of our modification. We wonder whether our method may avoid the complication related to cardiac tamponade reported by Cox [11] and Kosakai [18] and colleagues.
Study Limitations The first limitation of this study was that the atrial linear lesions created by radiofrequency energy were judged by discoloration. Because atrial electrograms were not recorded during the procedure, it was not certain whether the atrial discoloration represented a complete conduction block. However, the success rate of restoration of sinus or atrial rhythm was comparable with that of previous studies using a surgical approach. The mechanisms of AF have been postulated to involve single or multiple rapidly discharging foci [15, 24] or multiple wave front reentrant circuits [24]. Thus, the second limitation was the lack of mappings of AF to define the mechanisms. A mechanistic approach may allow a less extensive procedure but still achieve a high success rate [15, 16]. The third limitation was that this was a nonrandomized study in a small number of patients, making it difficult to compare with the classic surgical maze procedure. Further study with a larger number of patients should be conducted to confirm the feasibility of this method. In conclusion, a combination of radiofrequency linear ablation and cryoablation simulating the maze procedure during valvular operation is feasible and effective for achieving an acceptable success rate to restore sinus rhythm and atrial transport function in patients with chronic AF.
References 1. Chesebro JH, Fuster V, Halperin JL. Atrial fibrillation—risk marker for stroke. N Engl J Med 1990;323:1556– 8. 2. Coulshed N, Epstein EJ, McKendrick CS, Galloway RW, Walker E. Systemic embolism in mitral valve disease. Br Heart J 1970;32:26–34. 3. Rodriguez LM, Smeets JLRM, Xie B, et al. Improvement in left ventricular function by ablation of atrioventricular nodal
1672
4.
5.
6.
7.
8.
9. 10.
11.
12.
13.
CHEN ET AL CATHETER ABLATION OF ATRIAL FIBRILLATION
conduction in selected patients with lone atrial fibrillation. Am J Cardiol 1993;72:1137– 41. Coplen SE, Antman EM, Berlin JA, Hewitt P, Chalmers TC. Efficacy and safety of quinidine therapy for maintenance of sinus rhythm after cardioversion: a meta-analysis of randomized control trials. Circulation 1990;82:1106–16. Flaker GC, Blackshear JL, McBride R, Kronmal RA, Halperin JL, Hart RG, on behalf of the stroke prevention in atrial fibrillation investigators. Antiarrhythmic drug therapy and cardiac mortality in atrial fibrillation. J Am Coll Cardiol 1992; 20:527–32. Sato S, Kawashima Y, Hirose H, Nakano S, Matsuda H, Shirakura R. Long-term results of direct-current cardioversion after open commissurotomy for mitral stenosis. Am J Cardiol 1986;57:629–33. Hansen JF, Andersen ED, Olesen KH, et al. DC-conversion of atrial fibrillation after mitral valve operation: an analysis of the long-term results. Scand J Thorac Cardiovasc Surg 1979;13:267–70. Heinz G, Siostrzonek P, Kreiner G, Go¨ssinger H. Improvement in left ventricular systolic function after successful radiofrequency His bundle ablation for drug refractory, chronic atrial fibrillation and recurrent atrial flutter. Am J Cardiol 1992;69:489–92. Cox JL, Boineau JP, Schuessler RB, et al. Successful surgical treatment of atrial fibrillation. JAMA 1991;266:1976– 80. Feinberg MS, Waggoner AD, Kater KM, Cox JL, Lindsay BD, Pe´rez JE. Restoration of atrial function after the maze procedure for patients with atrial fibrillation: assessment by Doppler echocardiography. Circulation 1994;90(Suppl 2): 285–92. Cox JL, Boineau JP, Schuessler RB, Jaquiss RDB, Lappas DG. Modification of the maze procedure for atrial flutter and atrial fibrillation: I. Rationale and surgical results. J Thorac Cardiovasc Surg 1995;110:473– 84. Cox JL, Jaquiss RDB, Schuessler RB, Boineau JP. Modification of the maze procedure for atrial flutter and atrial fibrillation: II. Surgical technique of the maze III procedure. J Thorac Cardiovasc Surg 1995;110:485–95. Sandoval N, Velasco VM, Orjuela H, et al. Concomitant
Ann Thorac Surg 1998;65:1666 –72
14.
15.
16. 17. 18.
19. 20.
21. 22. 23.
24.
mitral valve or atrial septal defect surgery and the modified Cox-maze procedure. Am J Cardiol 1996;77:591– 6. Kawaguchi AT, Kosakai Y, Sasako Y, Eishi K, Nakano K, Kawashima Y. Risks and benefits of combined maze procedure for atrial fibrillation associated with organic heart disease. J Am Coll Cardiol 1996;28:985–90. Haı¨ssaguerre M, Marcus FI, Fischer B, Cle´menty J. Radiofrequency catheter ablation in unusual mechanisms of atrial fibrillation: report of three cases. J Cardiovasc Electrophysiol 1994;5:743–51. Haı¨ssaguerre M, Gencel L, Fischer B, et al. Successful catheter ablation of atrial fibrillation. J Cardiovasc Electrophysiol 1994;5:1045–52. Elvan A, Pride HP, Eble JN, Zipes DP. Radiofrequency catheter ablation of the atria reduces inducibility and duration of atrial fibrillation in dogs. Circulation 1995;91:2235– 44. Kosakai Y, Kawaguchi AT, Isobe F, et al. Modified maze procedure for patients with atrial fibrillation undergoing simultaneous open heart surgery. Circulation 1995;92(Suppl 2):359– 64. Boineau JP, Schuessler RB, Canavan TE, Corr PB, Cain ME, Cox JL. The human atrial pacemaker complex. J Electrocardiol 1989;22(Suppl):189–97. Kobayashi Y, Ohe T, Shimizu W, Kosakai Y, Shimomura K. Coexistence of normal sinus rhythm and atrial fibrillation on electrocardiogram after the maze procedure. Am Heart J. 1994;128:1045–7. Jordaens L, Missault L, Germonpre´ E, et al. Delayed restoration of atrial function after conversion of atrial flutter by pacing or electrical cardioversion. Am J Cardiol 1993;71:63–7. Kosakai Y, Kawaguchi AT, Isobe F, et al. Cox maze procedure for chronic atrial fibrillation associated with mitral valve disease. J Thorac Cardiovasc Surg 1994;108:1049–55. Holman WL, Ikeshita M, Ungerleider RM, Smith PK, Ideker RE, Cox JL. Cryosurgery for cardiac arrhythmias: acute and chronic effects on coronary arteries. Am J Cardiol 1983;51: 149–55. Moe GK, Abildskov JA. Atrial fibrillation as a self-sustaining arrhythmia independent of focal discharge. Am Heart J 1959; 58:59–70.