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Ann Thorac Surg 2003;76:836-842
© 2003 The Society of Thoracic Surgeons
a Division of Cardiothoracic Surgery, Washington University School of Medicine, St. Louis, Missouri USA
* Address reprint requests to Dr Damiano, Washington University School of Medicine, One Barnes-Jewish Plaza, Queeny Tower Suite 3108, St. Louis, MO 63110, USA
e-mail: damianor{at}msnotes.wustl.edu
Presented at the Thirty-eighth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2002.
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Abstract |
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METHODS: Five dogs underwent baseline pacing from the following target areas: right and left atrial appendage, superior and inferior vena cavae, and right and left pulmonary veins. A cuff of atrial myocardium, proximal to the target tissue was clamped and ablated between the arms of the bipolar radiofrequency energy device. Tissue conductance was used as a transmural indicator. After ablation, the pacing protocol was repeated. Baseline and postablation pulmonary vein flows were measured. Animals were survived for 30 days, and permanent electrical isolation was evaluated by pacing, epicardial mapping, and histology.
RESULTS: Mean ablation time was 5.0 ± 1.8 seconds and mean peak tissue temperature was 46.7°C ± 2.8°C. All lesions (30/30) acutely and permanently isolated atrial tissue. There was no change in pulmonary vein flow. Mapping studies with pacing of atrial tissue on both sides of the lesion confirmed isolation. Histology demonstrated that all lesions were linear, continuous, and transmural with no thrombus formation or stenosis.
CONCLUSIONS: Bipolar radiofrequency energy rapidly produced permanent transmural linear lesions on the beating heart. Measurement of tissue conductance reliably predicted transmural lesions. This new technology may enable the development of a less invasive, surgical approach to atrial fibrillation.
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Introduction |
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| Drs Schuessler and Damiano disclose that they have a financial relationship with AtriCure, Inc.
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Radiofrequency energy (RF) has been used in surgical operations for nearly a century. McLean [9] reports that Bovie introduced the first electrosurgical unit in 1928, and with technologic advances over the last several decades, applications for RF energy have been developed in virtually all medical and surgical specialties. Recent clinical studies in cardiac surgery have investigated the use of unipolar RF energy as an adjunct to atrial fibrillation (AF) surgery with varied success [10]. This may in part be due to the inability to confirm transmural lesions at the time of surgery. This study was designed to evaluate a new technology, bipolar RF energy. With this technology, radiofrequency energy is delivered between two electrodes rather than from a monopolar source. This results in a more focused delivery of energy, which potentially could minimize lesion width and collateral tissue injury. Another advantage of placing the tissue between two electrodes is that it becomes possible to measure real-time tissue conductance and energy delivery.
Conductance was hypothesized to represent a way to define precisely when the lesion became transmural. As the tissue is irreversibly desiccated, tissue conductance should fall and reach a stable minimum value. At this point, ablation can be stopped, minimizing unnecessary energy delivery. It was our hypothesis that bipolar RF energy could reproducibly create transmural lesions capable of chronically isolating atrial tissue in a rapid and controlled manner. This study examined the physiologic consequences of bipolar RF energy on the structure and integrity of the atrial myocardium and the pulmonary veins.
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Material and methods |
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Data acquisition: acute study
Prior to ablation, the heart was paced from the free wall of the right and left atria and the right and left atrial appendage, and at the junction of the atrium and the right and left pulmonary veins, and the superior and inferior vena cavae using a bipolar epicardial electrode. Pacing thresholds were recorded at all sites at a fixed pulse width of 0.5 ms. Pulmonary vein flows were recorded using a 4-mm ultrasonic flow probe (Transonics, Ithaca, NY) attached to a flow meter ([Model T206]), Transonics, Ithaca, NY). During flow measurements, ventilation was temporarily discontinued and the heart was paced at a constant rate of 100 bpm. Blood pressure was maintained at a mean of 40 mm Hg. Pre-ablation flows were recorded twice for 30 seconds from each of the four main pulmonary veins. After ablation, pulmonary vein flows were similarly recorded from the identical sites.
A bipolar RF ablation device was used to create the lesions (AtriCure Inc, Cincinnati, OH) (Fig 1). The bipolar hand piece consisted of two 5-cm long arms, each with an embedded 1-mm electrode. The RF generator was able to independently control both voltage and current delivery to the electrodes. A laptop computer with Labview version 5.1 (National Instruments, Austin, TX) was used to monitor and record temperature, time, current, voltage, impedance, conductance and energy delivered. Temperature was recorded by a themocouple 1 mm from the electrode edge. The computer system displayed these variables in a graphical format in real time. Atrial lesions were created by clamping a cuff of atrial tissue between the two electrode arms. (Fig 2) Radiofrequency energy was delivered at 75 volts and 750 milliamps. It was hypothesized that a steep fall in tissue conductance would be an indicator of transmurality. Therefore, the ablation was continued until the tissue conductance between the two electrodes decreased below 0.0025 Siemens and achieved a steady state for 2 seconds. (Fig 3) After ablation, bipolar pacing was performed from each of the previous sites. Electrical isolation was defined as the inability to capture the free wall of the atrium by pacing at stimulus strengths up to 20 mA.
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A custom 256-channel epicardial atrial mapping system was used to map the atria. The system has been previously described in detail [11]. Custom made silastic plaques were secured to cover the entire atrial epicardial surfaceFig. 4. These plaques contained 256 silver unipolar electrodes 1 mm in diameter with an inter-electrode distance of 5 mm. Data were recorded with a gain of 1,000 and a frequency response of 50 to 1,000 Hz. The electrode data were digitized at 1,000 Hz. Activation times were automatically determined by the maximum dV/dT of the unipolar deflection, and were manually edited for verification. Electrophysiologic data were recorded under four experimental conditions: (1) normal sinus rhythm; (2) pacing from the tip of the isolated right atrial appendage; (3) pacing from the tip of the isolated left appendage; and (4) pacing from the free wall of the right atrium.
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All animals received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH Publication No. 85–23, revised 1985).
Statistics
The data were expressed as mean ± standard deviation. The comparisons of ablation time, energy, and temperature were performed by the student’s t test.
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Results |
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Pulmonary vein flows
Pulmonary vein flow was documented from the four pulmonary veins of each animal before and after acute ablation. In animals with more than four total pulmonary veins, the two largest veins from each side were used. The average pre-ablation pulmonary vein flow was 226 ± 55 mL/min. After ablation, the average pulmonary vein flow was 213 ± 48 mL/min. There were no significant differences between acute pre-ablation and postablation flows.
Atrial mapping
Bi-atrial mapping at 30 days demonstrated complete circumferential lines of conduction block by each bipolar lesion. The cuffs of atrial myocardium surrounded by the ablation were completely isolated from the remainder of the heart. By recording data during both normal sinus rhythm and pacing from inside the completely isolated atrial tissue, bi-directional electrical isolation was documented in each animal.
Histology
At 30 days, gross examination of the atria, vena cava, and pulmonary veins revealed no evidence of thrombus or stricture formation (Fig 4). Of note, both the isolated right and left atrial appendages were viable with no evidence of necrosis. Both isolated appendages could be paced and were contractile. By microscopic examination, all lesions (30/30) were transmural, continuous, and discrete. Lesion width varied depending on tissue depth and the time of the lesion. In areas of thin walls (ie, inferior vena cava), the lesion width was fairly constant at 1 mm. On thicker areas of the atrium (ie, the appendage) where the wall thickness was up to 5 mm, the lesion width was greater but was never more than 2.5 mm. There was no evidence of endothelial proliferation or thrombus formation at the site of ablation. The pulmonary vein lesions demonstrated no stricture or luminal narrowing. The lesion widths on the pulmonary vein lesions were never wider than 1.5 mm (Fig 5).
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Comment |
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TopAbstractIntroductionMaterial and methodsResultsCommentDiscussionAcknowledgmentsReferences |
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Despite the proven long-term efficacy of the Cox-Maze III procedure, widespread adoption of this procedure has been limited by its length, technical difficulty, and prolonged cardiopulmonary bypass times [5]. The majority of patients in the United States undergoing mitral valve surgery with concomitant AF have been deprived of a curative operative procedure for AF because of the perceived complexity of the Cox-Maze procedure. Ablation technologies have been introduced in an attempt to facilitate the surgical treatment of atrial fibrillation by creating myocardial lesions that replace surgical incisions. By substituting linear lines of ablation for the traditional cut-and-sew approach, it has been hypothesized that the procedure could be performed more simply, potentially decreasing its morbidity, and making it more applicable to the entire spectrum of patients with AF.
Limitations of unipolar RF energy
None of the currently available unipolar RF devices are able to document real-time transmural lesions. Because of this limitation, it is necessary to use prolonged ablation times and multiple applications of energy to give the surgeon some reassurance of transmural ablation. High temperatures are needed at the tissue-electrode interface to insure penetration of the myocardium. This results in coagulum at the single electrode, which increases the resistance to the flow of energy [12]. This leads to the energy traveling laterally around the developing lesion instead of directly through the tissue. This uncontrolled, multidirectional flow of energy results in wider lesions and collateral tissue injury [13]. Unipolar RF energy has been shown to produce wide lesions ranging up to 1 to 2 cm [13]. There have also been reports of delayed esophageal perforation with the use of the unfocused unipolar RF energy during surgery for AF [14]. High temperatures also lead to protein denaturization in surrounding structures, including red blood cells and matrix proteins. Although this is an advantage for unipolar RF energy in certain organs, such as the liver in the prevention of bleeding, it is a drawback in myocardial tissue. In the heart this can lead to the formation of thrombus and subsequent embolization [15]. Contracture of the myocardial matrix, especially near the pulmonary veins can lead to stenosis. Previous studies have suggested that unipolar radiofrequency energy causes acute pulmonary vein injury leading to luminal narrowing, stenosis, thrombus formation, and even complete occlusion of the pulmonary veins [16, 17]. Admittedly, these complications have been reported during catheter ablation procedures. In contrast, the careful surgical use of unipolar RF energy to dry endocardial fields in the arrested heart has not been associated with a significant number of reported complications. It should be noted that most described surgical techniques have avoided energy application to the actual pulmonary vein orifices.
A final drawback of unipolar thermal ablation is the difficulty in obtaining transmural lesions on the beating heart. The circulating blood volume on the endocardial surface constitutes virtually infinite heat sink preventing the device from achieving the high ablation temperatures required for permanent tissue injury at the endocardial surface. Our laboratory has shown that unipolar RF is unable to create transmural lesions on the beating heart [18].
This study demonstrated the ability of bipolar radiofrequency energy to produce permanent transmural linear lesions on the beating heart. Moreover, several advantages of bipolar RF energy were clearly defined in our experiments. As opposed to other unipolar energy sources, lesion transmurality can be reliably correlated with an objective real-time endpoint. In this study, a drop of tissue conductance below 0.0025 Siemens for 2 seconds resulted in a 100% correlation with the development of a permanent transmural scar. By using this physiologic parameter of transmural ablation, ablation time can be tailored to the particular tissue characteristics as opposed to using an empirical method to derive ablation time or tissue temperature. The duration of bipolar RF ablation is determined by the thickness and resistivity of the tissue between the electrodes.
The ability to determine transmural ablation in real-time leads to several interwined advantages of bipolar RF ablation. First, the tissue receives just enough energy to produce a transmural lesion, shortening ablation time to seconds as opposed to minutes with other energy sources. By shortening ablation time, the duration that surrounding tissue is exposed to excessive resistive heating is reduced, thereby minimizing thermal spread to surrounding tissue and structures. Tissue temperature averaged only 40°C to 50°C 1 mm from the electrode edge as opposed to temperatures of 80°C to 90°C with other thermal ablation devices. By reducing thermal spread, only the tissue immediately adjacent to the electrode is exposed to the elevated temperatures required to produce necrosis and scarring. This limits the contracture of tissue to a few millimeters and removes the danger of stenosis or aneurysm formation. In this study the average lesion width was less than 2 mm as opposed to several centimeters as seen with some of the other devices.
Another advantage of bipolar RF energy is that the ablative energy is focused between the two electrodes. The current passes from one electrode to the other transversing through tissue in the shortest, least resistant path, and this results in discrete lesion widths of less than 2.5 mm. Moreover, this makes it difficult to injure surrounding structures (ie, coronary arteries, esophagus).
The lower temperatures and more discrete lesions may decrease the risk of both intraoperative and postoperative thromboembolic complications or stricture. No intracavitary thrombi were found in this chronic study. Moreover, there was also no evidence of pulmonary vein stenosis. This complication has been reported to be as high as 39% acutely and 8% chronically after transvenous catheter ablation using unipolar RF energy [16]. A potential benefit of the narrow discrete lesions may be better preservation of atrial transport function (a critical outcome measurement of the Cox-Maze procedure). However, this has yet to be proven.
Study limitations
There are several limitations of this device. It is not malleable and it can be difficult to maneuver in the chest. The adaptation of this bipolar RF energy ablator to a totally endoscopic approach will be difficult because of the rigidity of the electrode arms. The length of the instrument (5 cm) is adequate for canine lesions, but may be short for large human atria and pulmonary veins. A theoretical drawback in using bipolar technology is that it is possible to receive a false positive if there is air between the tissue and the electrode. Air will act as an insulator and will feed back to the computer system that the exposed portion of the electrode has a conductance below 0.0025 Siemens. Although it did not happen in this study, care must be taken to firmly clamp the tissue between the jaws of the device to eliminate this possibility. In addition, this study has the drawbacks of all animal studies in that direct extrapolation to the clinical situation must be done with caution. These animals had normal atria with thinner tissue and less fat than diseased human myocardium. Finally, there was no attempt to perform an entire Cox-Maze III procedure with this device. The ability of bipolar radiofrequency energy to fully replicate all the lesions of a Cox-Maze III procedure remains unknown.
In summary, the surgical treatment of AF has been established for more than a decade. The complexity of the surgery has limited its widespread application to all patients with atrial fibrillation. New technologies that simplify and shorten the operation by producing transmural lesions to replace the multiple surgical incisions of the Cox-Maze III procedure offer promise. This study documented the creation of permanent lines of electrical isolation in atrial myocardium with bipolar energy. Moreover, this novel technology can produce linear, transmural lesions in the beating heart. The measurement of tissue conductance as a real-time determinant of transmural lesions is one of the unique advantages of bipolar energy. Our results suggest that bipolar RF energy may be an enabling technology to allow surgeons to perform curative surgery for atrial fibrillation on the beating heart.
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Discussion |
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DR PRASAD: This is actually our fourth animal study with this type of technology. There have been previous chronic studies that did demonstrate that we actually have very similar lesions on the pulmonary veins themselves, which was presented at the American College of Surgeons, but one of the advantages of doing surgical isolation of the pulmonary veins is that we do not have to go on the pulmonary veins, we can actually isolate a cuff of atrial myocardium around the pulmonary veins and thereby isolate any sort of initiation in the pulmonary veins.
DR VERDI J. DISESA (West Chester, PA): Does this set of lesions cure atrial fibrillation?
DR PRASAD: No. This set of lesions was specifically designed so that we could maximize the number of lesions we could construct on the heart in areas we could document electrical isolation by pacing. So we used the atrial appendages and the vena cava and the pulmonary veins so that we had six lesion sets that were circumferential and we could pace from tissue within the isolated segment. This has nothing to do with any sort of lesion set to stop atrial fibrillation, although some would argue that PAF may be treated with isolated pulmonary vein isolation.
DR DISESA: But is not part of your argument that you can do this off pump with all epicardial lesions, and therefore it is a little disingenuous to put the two together without acknowledging that this is not an operation for atrial fibrillation?
DR PRASAD: Correct. What we have demonstrated in this study is not a curative operation for atrial fibrillation. What we have demonstrated is that we can reliably replace the surgical incisions that are done for the Maze procedure, or any sort of arrhythmia surgery procedure, with ablations, and that we may be able to place these lesions. We do have an ongoing study right now to actually confirm all the Cox-Maze III lesions on the beating heart in dogs. So that would be the final step.
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