Ann Thorac Surg 2008;85:1283-1289. doi:10.1016/j.athoracsur.2007.12.037
© 2008 The Society of Thoracic Surgeons
Original Articles: Adult Cardiac
Intraoperative Modified Cox Mini-Maze Procedure for Long-Standing Persistent Atrial Fibrillation
Yong Qiang Cui, MD, PhD,
Ling Bo Sun, MD, PhD,
Yan Li, MD,
Chun Lei Xu, MD,
Jie Han, MD,
Hui Li, MD,
Xu Meng, MD*
Atrial Fibrillation Center, Anzhen Hospital, Beijing, China
Accepted for publication December 11, 2007.
* Address correspondence to Dr Meng, Department of Cardiac Surgery, Anzhen Hospital, Beijing, 100029, China (Email: mxu{at}263.net).
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Abstract
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Background: As the most effective method of curing atrial fibrillation, the classic Maze III procedure eliminates atrial fibrillation in more than 90% of patients. In spite of high efficacy, the complexity and complications associated with this procedure prevents widespread application. In this research, we report our experience with a modified Cox mini-Maze procedure using radiofrequency energy for treating long-standing persistent atrial fibrillation during open-heart surgery.
Methods: A total of 45 patients with long-standing persistent atrial fibrillation who underwent open-heart surgery received the treatment. This modified Cox mini-Maze procedure was performed using unipolar and bipolar radiofrequency systems. Some lesions were done with unipolar pen both epicardially and endocardially to improve the transmurality of ablation.
Results: Hospital mortality was 0%. The follow-up time ranged from 6 to 26 months (mean, 16.6). Overall freedom from atrial fibrillation was 86.7% at latest follow-up after surgery. When analyzed by the Kaplan-Meier method, freedom from atrial fibrillation was 94% (6 months), 87% (12 months), and 82% (24 months). Compared with a randomized Cox Maze III control group, the results of freedom from atrial fibrillation do not show significant differences between the two groups at interval contacts. The survival rate was 100% (45 of 45), as was freedom from stroke. No patients required implantation of a permanent pacemaker. Recovery of atrial contractility occurred in 94.6% of patients (35 of 37) during the latest follow-up.
Conclusions: According to our experience, the modified Cox mini-Maze procedure allows rapid ablation application and offers an optimistic outcome for the recovery of sinus rhythm in patients with long-standing persistent atrial fibrillation who undergo open-heart surgery.
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Introduction
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Atrial fibrillation (AF) affects approximately 10 million patients in China [1]. Atrial fibrillation is associated with increased mortality, increased risk of stroke, and exacerbation of heart failure [2–4]. Antiarrhythmic medications have limited efficacy in maintaining sinus rhythm and may have serious adverse effects [5–7]. The 15-year success rate of the Cox Maze procedure has been reported to be as high as 97% for AF associated with other cardiac conditions such as mitral valve disease [8], although it has not been widely adopted because of the need to perform extensive incisions and suturing of the atriums, resulting in lengthy procedure and cross-clamp times [9]. Based on empirical clinical observation and other emerging evidence, Dr James Cox forwarded the new theory that many lesions in the Maze procedure can be eliminated and yet still cure continuous AF. He established this lesion pattern, referring to it as the Cox mini-Maze procedure [10]. This procedure contains the following lesions: pulmonary vein encircling incision, left atrial isthmus lesion with its attendant coronary sinus lesion, and right atrial isthmus lesion. As the logical streamlined descendent of the original Maze procedure, the Cox mini-Maze procedure aims at treating most patients with AF of either type.
Based on the concept of the Cox mini-Maze procedure, and our own experience [11] since September 2005, we started applying a modified mini-Maze procedure, which was incorporated with recent theoretical and clinical developments in the treatment of AF. This modified mini-Maze procedure includes a pulmonary vein encircling incision, connecting lesion of both pulmonary veins through the left atrial roof, another connecting lesion between superior vena cava and ascending aortic artery through the left atrial roof, left atrial isthmus lesion, coronary sinus lesion in both right atrium and left atrium, and right atrial isthmus lesion. Furthermore, dissection of the ligament of Marshall and partial epicardial ablation of autonomic ganglionic plexi are incorporated into this procedure.
Below we report our follow-up results for a long-standing persistent AF cure, discussing the influence of clinical and technical variables on the outcome.
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Patients and Methods
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Patient Selection
From September 2005, a total of 45 patients were enrolled. Indication for the concomitant treatment was long-standing persistent AF, which is defined as continuous AF of more than 1 year’s duration, according to the HRS/EHRA/ECAS Expert Consensus Statement [12]. The exclusion criteria were history of a cardiac procedure, AF patients who had undergone off-pump coronary bypass graft procedure, and emergency operation. All of the 45 patients were affected by mitral valve disease, with concomitant organic heart disease present in 29 cases (64%). One patient had had a previous stroke.
During the same period, another 40 cases of Cox Maze III (radiofrequency) were enrolled as a randomized control group. Relative data are summarized in Tables 1 and 2.
The Institutional Review Board approved the research protocol. Informed consent, including the cost of unipolar and bipolar ablation systems, was obtained from each patient.
Preoperative Management
Baseline 12-lead electrocardiogram, chest roentgenogram, and transthoracic ultrasonic cardiogram were obtained on admission. All patients were required to fill in a questionnaire about their AF history, antiarrhythmia drug use, New York Heart Association (NYHA) heart function, history of stroke, and so forth.
Operative Technique
The Cardioblate BP2 RF ablation systems (Medtronic, Inc, Minneapolis, Minnesota) were used in this study; they include both a bipolar clamp and a unipolar pen, and represent the most advanced radiofrequency (RF) ablation engineering in the field.
The Cox mini-Maze technique has been previously described [10]. The modified mini-Maze procedure differs in four aspects. (1) Connecting lesion of both pulmonary veins is made through the left atrial roof instead of left atrial posterior wall, and another connecting lesion of superior vena cava and ascending aortic artery through the left atrial roof epicardially, with the unipolar system. This modification not only avoids any damage to the esophagus, but also aims at blocking intra-atrial reentry circuits conducting through Bachmann’s bundle. The pulmonary veins connecting lesion is performed from both inside and outside of the left atrium to improve the transmurality of ablation. (2) Left atrial isthmus ablation: this lesion is made from the inferior aspect of the left pulmonary vein isolation lesion, to the mitral valve posterior annulus at approximately 6 o’clock position, with the unipolar pen. (3) Ablating the coronary sinus in both the right and left atrium: in the left atrium, with bipolar clamp, the ablation is placed from the inferior aspect of the left atrial incision, across the coronary sinus, toward the mitral valve posterior annulus where the left atrial isthmus lesion ends (6 o’clock position). This lesion should be made to intersect the lower segment of the left atrial isthmus lesion since it does not reach the mitral valve annulus. In the right atrium, with unipolar pen, a lesion is made from the orifice of coronary sinus to the tricuspid septal annulus. Care should be taken to avoid injury to the atrioventricular node. (4) The partial epicardial denervation technique, which consists of three steps: the first is both isolation and ablation of the ganglionic plexi around the pulmonary veins, with unipolar pen, according to the schematic diagram developed by Ben Sherlag and colleagues (provided by Atricure, Inc). The second is the physical dissociation of all visible fat pads from the surface of the interatrial groove. The third step is dissection of ligament of Marshall, plus the ablation of regional fat tissue along the limbus of ligament of Marshall.
The lesion set is shown in Figure 1.
Electrophysiologic Mapping
Intraoperative electrophysiologic testing was performed, which includes bilateral pulmonary vein antrum baseline and post–isolation sensing [13], pulmonary vein antrum baseline and post–isolation pacing. A baseline positive "sensing" (rapid and disorderly atrial potentials) in the pulmonary vein antrum area could be detected before pulmonary vein isolation, and a negative "sensing" (no atrial potentials) in the same area after ablation, which is called "entrance block." A positive baseline "pacing" is defined as the "atrial capture" is obtained. Capture is the contraction of the atrium in response to the electrical stimulus being sent from the temporary pacemaker (Oscor Pace 203H DDD External Dual-Chamber Pacemaker). A negative post–ablation "pacing" means that no capture is obtained in the same area after ablation. Combined positive baseline pacing and negative post–ablation pacing is called "exit block." Achieving both entrance and exit block is regarded as a transmural lesion blocking the conduction in the pulmonary vein antrum area. Meanwhile, a conduction block testing of the pulmonary vein connection lesion and left atrial roof lesion made by unipolar pen was also performed. Two pacing sites on the left atrial roof were set up before ablation. Also, two other sites on both side of one lesion were set up for sensing and detecting the impulses from the two pacing sites. A comparison of conduction durations from the pacing sites to the sensing sites was made before and after ablation; a prolongation of more than 80 ms was regarded as a conduction block of the certain lesion.
Postoperative Management and Follow-Up
Antiarrhythmic prophylaxis was carried out on a routine basis. Amiodarone (intravenous 300 mg, followed by a continuous infusion of 1, 200 mg in 24 hours until postoperative day 3; and oral administration of 200 mg every day until discharge) was administered to 45 patients (100%). After discharge, all patients were informed that amiodarone should be continued for at least 6 months and then be tapered off in the presence of a stable sinus rhythm. Betaloc (AstraZeneca Inc, London, UK) was also used combined with amiodarone postoperatively.
As far as ultrasonic cardiography is concerned, the sizes of the left ventricle, left atrium, and ejection fraction are routine index. Peak velocities of the early wave (E wave) and of the late filling wave (A wave) were determined as the average of three consecutive beats. A peak A wave velocity of 10 cm/s was arbitrarily considered as the cut-off for an effective atrial contraction [14].
Follow-up was obtained from office visits at the outpatient building, mailed medical records done at local hospitals, together with questionnaires. Results were evaluated at discharge, and at 3, 6, and every 6 months postoperatively. After 3 months, patients who were in sinus rhythm on electrocardiography underwent a Holter monitor. Free electrocardiographic examinations and free 24-hour Holter monitoring were offered at the AF Centre, Beijing Anzhen Hospital.
Statistical Analysis
Standard descriptive statistics were applied. Values are expressed as mean ± SD. Kaplan-Meier analysis was used for time-related freedom from AF. The Pearson 
2 test was applied to analyze the difference of success rate between this modified mini-Maze group and the Cox Maze III control group during the same period, based on rhythm at interval contacts. All p values are two tailed.
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Results
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Operative Results, Morbidity, and Mortality
Patient characteristics of both the modified mini-Maze group and the Cox Maze III comparison group are detailed in Table 1. There were no significant statistical differences between the two groups in terms of age, AF duration, left atrium dimension, and heart function. Open-heart procedures performed in the modified mini-Maze group are summarized in Table 2.
The technique was successfully completed in all patients. The mean ablation duration was 12.4 ± 3.9 minutes, significantly shorter than for the Cox Maze III group (19.5 ± 2.8 minutes; p < 0.05). No patients had ablation-related complications. Mean total bleeding was 370 ± 120 mL. No patients required reexploration for bleeding. Mean intensive care unit stay was 1.4 days. The majority of patients were discharged within 14 days (7.8 ± 3.9) after the operation.
The mean follow-up time is 16.6 ± 5.2 months (range, 6 to 26). Forty of the 45 patients (89%) continued taking coumadine since operation. Five (11%) are taking aspirin after 6 months of coumadine, as sinus rhythm was restored. Forty of 45 patients (89%) continued taking amoidarone within 1 to 6 months of follow-up. Although suggestion was made of 6-month’s continuous use at discharge, 5 of 45 patients (11%) stopped amoidarone at 1 to 3 months by themselves (3 of 5 patients) or suggested by local cardiologists (2 of 5), owing to "very low" heart rate (according to telephone record) or inability to get it at local hospitals (Fig 2).
Up to the latest follow-up, overall survival was 100%. No patients required implantation of a permanent pacemaker. The actuarial freedom from stroke was 100%. In the Cox Maze III group, 1 of 40 patients (2.5%) died of brainstem hemorrhage at 3 months after operation.
Patient outcomes in the modified Cox mini-Maze group are summarized in Table 3.
Heart Rhythm
All 45 patients had a total of 194 electrocardiograph examinations during follow-up (mean, 4.3 per patient). Twenty-four–hour Holter monitoring was done in 37 patients, and 48-hour Holter monitoring was done in 1 patient (Fig 3). Among the 14 patients discharged in AF, 2 patients had cardioversion at 2 and 3 months, respectively. Both of them remained in sinus rhythm at the latest follow-up. Four of the 6 patients (66.7%) who ultimately failed were the ones who were in AF at discharge.
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Fig 3. Frequencies of electrocardiographic (ECG) monitoring (dark gray boxes) and Holter monitoring (light gray boxes) during follow-up.
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Intraoperative electrophysiologic mapping was done for 17 patients in this study, including 8 patients who had pulmonary vein connection lesion and left atrial roof lesion (unipolar pen) testing. In the latter 8 patients, 6 (75%) had positive conduction block after ablation. Among 17 patients, 12 (71%) obtained both entrance and exit block of bilateral pulmonary vein isolation. Among them, during the latest follow-up, 11 of the 12 patients who had both intraoperative entrance and exit block were in sinus rhythm, and 3 of the 5 patients who did not gain both entrance and exit block were in sinus rhythm.
Overall, 31 of 45 patients (68.9 %) were free from AF upon discharge from hospital. At 3 months, 39 of 45 (86.7%) were in sinus rhythm. At 6 months, 40 of 45 (88.9%) were in sinus rhythm. At 12 months, 31 of 34 (91.2%) had restored sinus rhythm. At 18 months or longer, 12 of 14 (85.7%) were in sinus rhythm. Compared with the Cox Maze III group, the results of freedom from AF (rhythm at interval contact) of the modified Cox Maze group do not show significant differences at interval contacts (2 test; p = 0.822, 0.451, 0.629, 0.848, 0.798, 0.716, respectively; Fig 4).
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Fig 4. Percentage of patients in sinus rhythm in both groups at interval contact. (Lighter shaded bars = modified mini-Maze; darker shaded bars = Cox Maze III.)
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Overall freedom from atrial fibrillation was 86.7% at latest follow-up after surgery. When analyzed by the Kaplan-Meier method, freedom from AF was 94% at 6 months, 87% at 12 months, and 82% at 24 months (Fig 5).
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Fig 5. Kaplan-Meier curve demonstrating freedom from atrial fibrillation (AF) in patients who have undergone the modified mini-Maze procedure.
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Atrial Contractility
During the latest follow-up, 37 of the 39 patients in sinus rhythm came to Beijing Anzhen Hospital for a check-up. Among them, atrial contraction was detected by transthoracic ultrasonic cardiography. Considering a peak A wave velocity of 10 cm/s as the cut-off for an effective atrial contractility, among these 37 patients, 94.6% (35 of 37) regained atrial transport function.
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Comment
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In the past decade, the Cox Maze procedure proved to be the most effective treatment option for AF. Theoretically, this procedure was designed to preclude and, furthermore, cut off the macroreentry anywhere and everywhere in the atria. There is emerging evidence, however, that although continuous AF is maintained by multiple macroreentrant circuits, there might be a limited number of sites in the left atrium that are capable of sustaining such circuits [15]. According to Cox’s observation [10], many of the lesions of the original surgical Maze III procedure might not be absolutely essential for the ablation of AF. After the first report by Sueda and colleagues [16] on left atrial procedures for AF associated with mitral valve disease, there has been a growing interest in the development of modification of the Maze procedure, such as approaches limited to the left atrium, allowing a simple and quick resolution of associated AF [17–19]. In that case, it would be necessary to place lesions in only a few specific sites in the atrium. For example, percutanous pulmonary vein isolation has proved to be effective for most paroxysmal AF [20]. It also supports the surgical observation that many of the lesions in the Maze procedure can be eliminated and yet still cure continuous AF.
Based on the principles above, Cox developed the procedure of Cox mini-Maze in 2003 [10]. We first started performing the Cox Maze III procedure in 2002 using a unipolar RF system (Cardioblate) in China. There had been more than 300 cases treated intraoperatively at the AF Centre, Beijing Anzhen Hospital, with a reported overall success rate of 79% [11]. Until now, more than 600 cases have been included. Based on the recent 4 years’experience, some simple but special techniques have been developed with the possibility of improving treatment outcomes to a certain extent.
First, we apply both endocardial and epicardial ablation of a same lesion with the unipolar RF pen. It is always a disturbance in term of transmurality with a unipolar ablation device (RF, microwave, laser, and so forth) as there is no objective evidence that transmurality is achieved. So ablating a lesion from both inside and outside the atrium can improve the transmurality of lesions. The versatility and malleability of the unipolar pen with its electrode tip allowed us to utilize this technique for ablation. Using a bipolar RF clamp, tissues are compressed between the jaws of the clamp and energy is delivered. Although the bipolar RF clamp can ensure transmurality, especially when it has a transmurality feedback algorithm, the jaws of the device cannot be used to ablate in the same pattern suggested by the diagram of the modified mini-Maze procedure, like left atrial roof lesions. Moreover, if the left atrium is enlarged, the bipolar device may not completely encircle the pulmonary veins. Using this endocardial and epicardial technique, the unipolar pen has the potential to overcome this shortcoming and can be used to create all of the recommended ablations with continuity and conduction block, in a simple and effective manner. In this study, electrophysiologic study testified the validity of the bipolar clamp, and the endocardial and epicardial technique with the unipolar pen. Transmural and continuous lesions are the key for surgical ablation of AF, which in this study contributes to the optimistic follow-up outcomes.
Second, we remove the connecting lesion of both the pulmonary vein islands on the posterior wall up to the left atrial roof, with the new lesion still connecting the two pulmonary vein circular ablations, and an attendant epicardial lesion connecting the roots of both superior vena cava and ascending aortic artery through the left atrial roof. One advantage of this change is that the most common adjacent esophageal injury can be totally avoided; the other reason is that the reentry circuits and conduction around Bachmann’s bundle [21], which is distributed through the left atrial roof, can also be ablated. We got this idea from two intraoperative electrophysiological mapping practice with ESI systems (Endocardial Solutions, St. Paul, Minnesota) [22]. During the operations, after the standard left atrial lesions (Cox Maze III) were applied, the mapping result still showed that there was a dominant reentry spread from the left superior pulmonary vein, through the left atrial roof, down to the right atrium. So we added an additional endocardial lesion at the left atrial roof, and the reentry was precluded immediately. At 6 month’s follow-up, the patient was in stable sinus rhythm. Haissaguerre and colleagues [23] recently studied the relative contributions of different atrial regions to the maintenance of persistent AF. Their results showed that among all the critical structures for termination of AF, ablation lesions at the left atrial roof (10%) had a vital impact on termination of AF, compared with pulmonary veins (18%).
Third, we did the ablation of coronary sinus from both right and left atria. As for surgical ablation of coronary sinus, cryothermy has been a traditional option [24]. But compared with cryothermy, the energy that a unipolar RF pen delivers is just confined within the pen tip and cannot spread widely. Therefore, the coronary sinus ablation is done from both atria, in an attempt to improve the transmurality and also widen the ablative portion of coronary sinus.
Fourth, we performed partial epicardial denervation, theoretically to enhance the outcome of this procedure. New mechanisms are currently being investigated as potential targets for both surgery and catheter ablation. The autonomic nervous system could play a role in triggering and maintaining AF. This has been known clinically for a long time, but only recently has vagal ganglia ablation become a new ablative strategy. According to Mehall and colleagues [13], more than 50% of ganglionic plexi are clustered around the interatrial groove and the ligament of Marshall. In this research, the three-step epicardial denervation procedure aims at these critical regions with easy and rapid application. Clinical variables such as hospital mortality, bleeding and other major complications, intensive care unit and hospital length of stay, and survival demonstrate the absence of any relevant impact of this procedure on normal postoperative recovery from open-heart surgery. On the contrary, combined with both unipolar and bipolar RF systems, the application of this modified mini-Maze procedure is very convenient, as it limits the additional cardiac arrest time required for open-heart ablations to aproximately 10 minutes, which was significantly shorter than for the Cox Maze III control group.
In our experience, recovery of left atrial contractility occurred in 94.6% patients who had atrial contraction detection by ultrasonic cardiography during the latest follow-up. In our opinion, this result was due to the myocardium preserving nature of the lesion set adopted. Only a refined strip of left atrial myocardium around each pair of pulmonary veins is electrically excluded with a bipolar RF clamp, and other limited numbers of lesions during the procedure would mean that minimization of myocardial exclusion and scarring plays a major role in favoring left atrial function recovery. But owing to technical reasons, the tricuspid flow was not detected in all the patients. Although we did see right atrial contraction in operations when sinus rhythm was restored after the modified mini-Maze procedure, there was no evidence showing that effective right atrial contractility was also recovered during the postoperative follow-up, considering that only a right-isthmus lesion was put in the right atrium.
In conclusion, this modified mini-Maze procedure allows good recovery of sinus rhythm and atrial function in the great majority of patients with AF who are having concurrent open-heart surgery. Based on the latest concepts in treating AF and certain modifications of traditional surgical ablative technique, it is a safe and effective means to treat AF, with limited technical and time requirements.
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Acknowledgments
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We would like to thank Shuping Ding for her assistance in data collection.
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References
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Abstract
Introduction
