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Nahush A. Mokadam
Patrick M. McCarthy
William H. Ryan
Marc R. Moon
Michael J. Mack
Sydney L. Gaynor
Sunil M. Prasad
Marci S. Bailey
Yosuke Ishii
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Ralph J. Damiano, Jr
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Ann Thorac Surg 2004;78:1665-1670
© 2004 The Society of Thoracic Surgeons

ORIGINAL ARTICLE: CARDIOVASCULAR

A Prospective Multicenter Trial of Bipolar Radiofrequency Ablation for Atrial Fibrillation: Early Results

Nahush A. Mokadam, MDa, Patrick M. McCarthy, MDb, A. Marc Gillinov, MDb, William H. Ryan, MDc, Marc R. Moon, MDa, Michael J. Mack, MDc, Sydney L. Gaynor, MDa, Sunil M. Prasad, MDa, Samuel A. Wickline, MDa, Marci S. Bailey, RNa, Nicholas R. Damianoa, Yosuke Ishii, MDa, Richard B. Schuessler, PhDa, Ralph J. Damiano, Jr, MDa,*

a Division of Cardiothoracic Surgery, Barnes-Jewish Hospital, Washington University School of Medicine, St. Louis, Missouri, USA
b Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
c Cardiopulmonary Research Science and Technology Institute, Dallas, Texas, USA

Accepted for publication May 12, 2004.

* Address reprint requests to Dr Ralph Damiano, Division of Cardiac Surgery, Washington University School of Medicine, Barnes-Jewish Hospital, One Barnes-Jewish Plaza, Suite 3108 Queeny Tower, St. Louis, MO 63110 (E-mail: damianor{at}msnotes.wustl.edu).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
BACKGROUND: The Cox-Maze III remains the gold standard for the surgical treatment of atrial fibrillation. However, the "cut-and-sew" technique is time consuming and technically challenging. The pulmonary veins are the source of ectopy in the majority of patients with atrial fibrillation. The safety and efficacy of bipolar radiofrequency to electrically isolate the pulmonary veins was evaluated in a prospective multi-center trial.

METHODS: Beginning in January 2002, 30 patients at three medical centers underwent pulmonary vein isolation using bipolar radiofrequency and were followed for 6 months. Twenty-four of the patients also underwent a modified Cox-Maze III. Electrical isolation of the pulmonary veins was confirmed with intraoperative pacing. Pulmonary vein patency was assessed by magnetic resonance imaging or three-dimensional computed tomography in 15 patients at 1 month.

RESULTS: Mean age was 60.9 ± 11.7 years. Nineteen patients had paroxysmal atrial fibrillation. All pulmonary veins were isolated in every patient. The left pulmonary veins underwent 3.0 ± 1.4 applications for a total of 26.4 ± 10.5 seconds. The right pulmonary veins underwent 2.8 ± 1.1 applications for a total of 26.3 ± 12.6 seconds. There was no operative mortality. At 1 month, imaging revealed no evidence of pulmonary vein stenosis. At 6 months, 96% of patients were in normal sinus rhythm.

CONCLUSIONS: The use of bipolar radiofrequency for electrical isolation of pulmonary veins and to replace other Cox-Maze III incisions is safe and effective at controlling atrial fibrillation. This emerging technology may shorten and simplify the surgical management of atrial fibrillation.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Atrial fibrillation affects more than 2.2 million people in the United States with approximately 160,000 new cases per year [1]. The morbidity associated with atrial fibrillation includes patient discomfort and anxiety caused by the tachyarrhythmia, hemodynamic compromise secondary to loss of atrial contraction, and thromboembolic complications, as a result of stasis in the left atrium [2–5]. Current management of atrial fibrillation includes antiarrhythmic drugs, cardioversion, percutaneous transcatheter ablation, and surgery. Although drugs can induce chemical cardioversion, their failure rate in some series is as high as 60% at 2 years [6]. When cardioversion fails, the use of chronic anticoagulation for stroke prevention has significant associated morbidity. Because the pulmonary veins have been shown to be the source of ectopic foci in many patients with paroxysmal atrial fibrillation, the use of catheter-based ablation and isolation of the pulmonary veins has gained popularity [7–9]. In particular, radiofrequency (RF) energy has been useful as it produces myocardial necrosis and can be delivered transvenously. Catheter-based unipolar applications have some limitations, including high tissue temperatures (90°C) and resultant collateral tissue damage. Although RF energy by endocardial application has met with good short-term success, long-term results have demonstrated a significant recurrence rate and a defined incidence of pulmonary vein stenosis [7, 10–13].

The Cox-Maze III procedure, first performed in 1988, involved the creation of a myriad of incisions, in both the right and left atria, to interrupt macro-reentrant circuits felt to be responsible for atrial fibrillation [14]. Long-term results have been outstanding with this procedure, with a freedom from atrial fibrillation of 97% at a median of 5.4 years and operative mortality less than < 2% [15, 16]. Unfortunately, the long-term benefits are offset by perioperative morbidity and mortality. This procedure is difficult to perform, and consequently, few surgeons have become proficient with this "cut and sew" technique. Because of these shortcomings, numerous authors have developed strategies to simplify this procedure.

Experimental work has demonstrated that bipolar RF energy is a promising ablation technology that can safely and effectively replace surgical incisions [17, 18]. The bipolar RF device used to perform ablations was manufactured by Atricure, Inc. (Cincinnati, OH). With this device, bipolar RF energy is delivered between two electrodes (5-cm length, 0.12-in width) mounted on the jaws of a specially designed clamp (Fig 1). When the clamp is closed on the target tissue, the electrodes are brought into close contact and energy is delivered in a focused and defined manner. The measurement of tissue conductance gives a reliable indicator of transmurality. In animal studies, it was found that when conductance reached a stable minimum, lesions were always transmural [17, 18]. Moreover, transmural ablations were able to be formed in seconds as opposed to the minutes required for unipolar energy sources. The lesions were discrete (1 to 2 mm in width) and there was little lateral spread of thermal energy, thus eliminating the risk of collateral damage to vital structures [17]. These experimental results suggested that bipolar RF ablation was an excellent energy source for the surgical treatment of atrial fibrillation. The purpose of this prospective multicenter trial was to evaluate the safety, efficacy, and intermediate-term results of using RF ablation to replace some of the incisions of the Cox-Maze III, and, in particular, for pulmonary vein isolation.



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  		Fig 1. The bipolar radiofrequency clamp.

 

   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Study Design and Endpoints
The study was designed as a prospective multicenter trial for patients undergoing pulmonary vein isolation with or without a concomitant Cox-Maze III procedure to evaluate the effectiveness of bipolar RF ablation to reproducibly create lesions on the atria that may replace the traditional surgical incisions. The primary endpoints of this study were: successful pulmonary vein isolation as evaluated by intraoperative pacing thresholds; presence of postoperative pulmonary vein stenosis on magnetic resonance imaging or three-dimensional computed tomography; and postoperative cure of atrial fibrillation. Secondary endpoints were bipolar RF energy application time, aortic cross-clamp time, cardiopulmonary bypass time, postoperative length of stay, postoperative arrhythmia, and major postoperative events (myocardial infarction, bleeding, stroke or thromboembolism). Follow-up was obtained at 1 and 6 months postoperatively.

Patient Accrual
Patients were enrolled after informed consent was obtained for their elective cardiac procedures. A written study protocol was submitted and approved by the institutional review boards at each of the participating institutions.

INCLUSION CRITERIA
The inclusion criteria for this study were: elective procedure, informed consent, indication for pulmonary vein isolation, atrial fibrillation for greater than 6 months, age between 18 and 80 years old, and ejection fraction greater than 30%.

EXCLUSION CRITERIA
The exclusion criteria were: prior cardiac surgery, serum creatinine greater than 2.0, ischemic mitral regurgitation, New York Heart Association (NYHA) class IV (congestive heart failure), carotid stenosis greater than 80%, myocardial infarction within the last month, active infection, severe peripheral arterial occlusive disease, pregnancy and nursing, substance addiction, and incompetence or other conditions preventing the patient from understanding the nature, significance, and scope of the study.

Bipolar Radiofrequency Ablation
The bipolar RF system consisted of the ablation sensing unit and the Atricure Isolator (Atricure, Inc., Cincinnati, OH). Using alternating current, this device produces a coagulative thermal injury by achieving local tissue temperatures in excess of 60°C. The energy is applied at 75W and 750mA between the jaws of the instrument. The generator continuously monitored voltage, current, temperature, time, and conductance. Tissue temperature was measured 1 mm from the electrode edge. Two seconds after conductance fell below 0.025 Siemens, an indicator light flashed and an audible tone was heard, signifying full thickness coagulation. The ablation sensing unit recorded total ablation time and maximum tissue temperature.

Operative Technique
Following median sternotomy and pericardiotomy, patients were placed on cardiopulmonary bypass. Intraoperative direct-current cardioversion was performed to obtain a normal sinus rhythm, if necessary. The right and left pulmonary veins were carefully dissected using a blunt technique. Bipolar epicardial pacing was performed from the right and left pulmonary veins, and pacing thresholds were obtained. Pulmonary vein isolation was performed at the beginning of the procedure. The bipolar RF clamp was then placed around the orifice of the right pulmonary veins. The clamp was closed such that a rim of atrial tissue was incorporated around the pulmonary veins. Following ablation, pacing thresholds were once again obtained. Bipolar pacing again was attempted up to 20mA from the both superior and both inferior pulmonary veins and recorded on the atrium to ensure electrical isolation. If atrial capture was documented, the ablation was repeated until electrical isolation was complete. This procedure was repeated for the left pulmonary veins. The patient then underwent the remainder of the operative procedure. In six patients, pulmonary vein isolation alone was performed as the sole treatment for atrial fibrillation, based upon the operating surgeon's judgment. Twenty-four patients underwent a modified Cox-Maze III procedure for the treatment of their atrial fibrillation, as depicted in Figure 2. Cryoablation with liquid nitrous oxide was used at the discretion of the operating surgeon at the tricuspid and mitral annuli and over the coronary sinus. Concomitant procedures performed in this study are listed in Table 1.



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  		Fig 2. (A) Posterior view of the atrium depicting the lesions created to perform the Cox-Maze III. (B) Intra-atrial view of Cox-Maze III lesions. (IVC = inferior vena cava; lt = left; RF = radiofrequency; rt = right; SVC = superior vena cava.)

 

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  		Table 1. Patient Characteristics and Procedures
 
Postoperative Care and Patient Follow-Up
Postoperatively, standard medical care was provided. At 1-month follow-up, a history and physical exam, an electrocardiogram, and an imaging study were obtained. At 6 months follow-up, a history and physical and an electrocardiogram were obtained. Anticoagulation and antiplatelet agents were administered as medically indicated. In most patients, antiarrhythmics drugs were administered routinely for the first 2 to 3 months. These were discontinued at the discretion of the individual physicians. Most patients were also anticoagulated with warfarin for the first 2 to 3 months.

Imaging Protocol
Electrocardiogram-gated, coil-enhanced magnetic resonance imaging with multiplanar reconstruction or high resolution computed tomography with three-dimensional reconstruction was used at 1 month to evaluate pulmonary vein anatomy in the first 15 patients. All four pulmonary vein orifices were identified in each study. The pulmonary vein diameters were correlated with clinical features to determine the presence or absence of pulmonary vein stenosis.

Statistics
Statistical analysis was conducted after entry into a confidential patient database. Data are expressed as percentages of totals and means with standard deviation.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Footnotes
 Acknowledgments
 References
 
Patient Enrollment and Demographics
Beginning in January 2002, a total of 37 patients were enrolled in the study. The centers included Washington University/Barnes-Jewish Hospital in St. Louis, MO (n = 19), Cleveland Clinic Foundation in Cleveland, OH (n = 13), and the Cardiopulmonary Research Science and Technology Institute in Dallas, TX (n = 5). Seven patients enrolled in the study did not complete the protocol. Two patients did not have the bipolar device used intraoperatively (surgeon choice), 3 patients did not have thresholds recorded, 1 patient was unable to be cardioverted into sinus rhythm, and 1 patient could not be paced intraoperatively. An analysis was performed on 30 patients. Four patients were not available for complete follow-up. One patient died after suffering a pulmonary embolus on postoperative day 48. Three patients declined their follow-up visits at 1 and 6 months secondary to long travel times. The clinical, electrocardiographic, and operative characteristics are outlined in Table 1.

Perioperative Results
Electrical isolation of the pulmonary veins as documented by pacing was successful in all patients. There were neither intraoperative complications nor intraoperative mortality. Intraoperative data are summarized in Table 2. Total ablation time for bilateral pulmonary vein isolation was 52.0 ± 17.2 seconds. The maximum tissue temperature 1 mm from the electrodes averaged 51.6°C ± 9.7°C. The peri-operative course of these patients included a median intensive care unit length of stay of 2 days (range 1 to 23 days). The median postoperative hospital length of stay was 12 days (range 5 to 30 days). Perioperative complications included intrathoracic bleeding requiring re-exploration in 13% (4 patients) and pacemaker placement in 13% (4 patients). None of the patients suffered a transient ischemic attack, cerebrovascular accident, deep sternal wound infection or myocardial infarction.


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  		Table 2. Intraoperative Data
 
Postoperative Results
Ninety-six percent of patients were in normal sinus rhythm at 6 months. Postoperative medicine usage is summarized in Table 3. Overall antiarrhythmic usage was 23% at 6 months.


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  		Table 3. Postoperative Drug Usage (Percent)
 
Imaging
Magnetic resonance imaging was obtained on 9 patients and three-dimensional computed tomography was obtained on 6 patients at their 1-month postoperative visit. There was no evidence of pulmonary vein stenosis on any of the patients (Fig 3).



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  		Fig 3. Magnetic resonance image depicting the right inferior pulmonary vein (arrow). There is no evidence of pulmonary vein stenosis.

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Footnotes
 Acknowledgments
 References
 
Recent studies have shown that the pulmonary veins play an integral role in the generation and persistence of atrial fibrillation [7–9]. Catheter-based techniques have been developed to electrically isolate the pulmonary veins. While these percutaneous procedures have had success, they have limitations. These have included a high recurrence rate of atrial fibrillation (possibly secondary to an inability to produce transmural lesions) [9–11], technical difficulty in isolation of some pulmonary veins [12], long fluoroscopy exposures [12], and the development of pulmonary vein stenosis [7, 10, 11, 19]. Although pulmonary vein stenosis can be palliated by interventional and surgical techniques (eg, balloon dilatation, stent placement), it remains a morbid complication. This study was designed to prospectively investigate surgical epicardial isolation of the pulmonary veins with a new technology, bipolar RF energy.

Bipolar RF energy was chosen over the other unipolar energy sources that are presently available for several reasons. It was the only FDA-approved energy source in which it was possible to determine lesion transmurality [17]. Moreover, the focused delivery of energy minimizes the chance of collateral damage that has been reported with unipolar, unfocused energy sources [19–21]. Finally, transmural ablations can be performed in seconds as opposed to minutes required for other devices.

In this multicenter trial, bipolar RF energy was capable of rapidly and reliably producing pulmonary vein isolation. Total ablation time was less than a minute and there were no device or ablation-related complications. There were no instances of collateral tissue damage in this small series. More importantly, bipolar RF energy did not produce pulmonary vein stenosis in any of the patients undergoing postoperative imaging.

Emerging technology has allowed the use of alternative energy sources to replace some of the incisions of the traditional "cut and sew" technique of the Cox-Maze III procedure [22, 23]. The challenge presented to all of these new technologies is to adequately replace the surgical incisions. They must be able to create discrete transmural lesions to assure conduction block. This has been a problem with some unipolar devices, due to the effect of convective cooling in the beating heart, variable catheter-to-tissue contact, and char formation [24–27].

This bipolar RF technology has the potential to overcome many of these limitations. Bipolar RF energy was able to routinely isolate the pulmonary veins on the beating heart in this study. Combined with the absence of pulmonary vein stenosis at 1 month, data from this study strongly support the safety and efficacy of bipolar RF ablation for surgical isolation of the pulmonary veins.

In 24 of the 30 patients in this study, the bipolar RF device was used to replace approximately half of the surgical incisions of the Cox-Maze III procedure. In the 23 patients who completed follow-up, the freedom from atrial fibrillation at 6 months was 96%. This was similar to the results obtained in a larger cohort of patients from Washington University who have undergone a traditional "cut and sew" Cox-Maze III procedure [15]. These preliminary results are encouraging, and further clinical investigation is clearly warranted to evaluate long-term efficacy.

Pulmonary vein isolation alone was performed in 6 patients. This was done at the discretion of the operating surgeons. The freedom from atrial fibrillation at 6 months in 4 patients for whom follow-up was available was 100%, as compared to 83% for catheter-based ablation, suggesting that this may be a viable option in highly selected patients [12].

The limitations of this study include its relatively small size and short follow-up. Particularly, imaging at 1 month may have been too soon to evaluate for late pulmonary vein stenosis. It is also acknowledged that only the first 15 patients underwent postoperative imaging. These evaluations were stopped once it became apparent that there were no stenoses. This remains, however, one of the few studies to carefully examine patients for pulmonary vein stenoses using sensitive radiographic imaging modalities, as opposed to less sensitive echocardiographic techniques.

Bipolar RF also has its limitations. Multiple applications were often required to isolate the pulmonary veins. This was felt to be due to the large amount of atrial tissue compared to the relatively small (5 cm) length of the clamp. Clearly, any bunching of tissue or air within the clamp could give a false-positive indication of transmurality. Because of this, pulmonary vein pacing is essential in all patients undergoing bipolar RF ablation to document transmural isolation.

Although further clinical investigation is warranted to evaluate the long-term efficacy of this technology in the treatment of atrial fibrillation, this study is one of the only prospective, multicenter trials of the surgical therapy for the treatment of atrial fibrillation. It was designed to evaluate the ability of bipolar RF energy to effectively isolate the pulmonary veins without causing stenosis. The results of this multicenter trial support the use of bipolar RF energy to isolate the pulmonary veins, thus replacing the surgical incisions of the Cox-Maze III procedure. Bipolar RF ablation has the potential to simplify the surgical treatment of atrial fibrillation. This may decrease the morbidity and increase utilization of curative atrial fibrillation surgery.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
References
 
Funded in part from an educational grant from Atricure, Inc., Cincinnati, OH, National Institutes of Health Grant No. RO1-HL032257, and National Institutes of Health Grant No. T32-HL007776.


   Footnotes
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
Acknowledgments
 References
 
Drs R. Damiano, McCarthy, Gillinov, and Schuessler disclose that they have a financial relationship with Atricure, Inc.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 

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  8. Haissaguerre M, Jais P, Shah DC, et al. Spontaneous initiation of atrial fibrillation by ectopic beats originating in the pulmonary veins N Engl J Med 1998;339:659-666.[Abstract/Free Full Text]
  9. Haissaguerre M, Shah DC, Jais P, et al. Electrophysiological breakthroughs from the left atrium to the pulmonary veins Circulation 2000;102:2463-2465.[Abstract/Free Full Text]
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  11. Robbins IM, Colvin EV, Doyle TP, et al. Pulmonary vein stenosis after catheter ablation of atrial fibrillation Circulation 1998;98:1769-1775.[Abstract/Free Full Text]
  12. Oral H, Knight BP, Tada H, et al. Pulmonary vein isolation for paroxysmal and persistent atrial fibrillation Circulation 2002;105:1077-1081.[Abstract/Free Full Text]
  13. Oral H, Knight BP, Ozaydin M, et al. Clinical significance of early recurrences of atrial fibrillation after pulmonary vein isolation J Am Coll Cardiol 2002;40:100-104.[Abstract/Free Full Text]
  14. Cox JL, Boineau JP, Schuessler RB, et al. Successful surgical treatment of atrial fibrillationreview and clinical update JAMA 1991;266:1976-1980.[Abstract/Free Full Text]
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  18. Prasad SM, Maniar HS, Diodato MD, Schuessler RB, Damiano Jr RJ. Physiological consequences of bipolar radiofrequency energy on the atria and pulmonary veinsa chronic animal study Ann Thorac Surg 2003;76:836-842.[Abstract/Free Full Text]
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Nahush A. Mokadam
Patrick M. McCarthy
William H. Ryan
Marc R. Moon
Michael J. Mack
Sydney L. Gaynor
Sunil M. Prasad
Marci S. Bailey
Yosuke Ishii
Richard B. Schuessler
Ralph J. Damiano, Jr
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