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Ann Thorac Surg 2006;81:72-76
© 2006 The Society of Thoracic Surgeons

Original article: Cardiovascular

Microwave Ablation for Atrial Fibrillation: Dose-Response Curves in the Cardioplegia-Arrested and Beating Heart

Sydney L. Gaynor, MD, Gregory D. Byrd, BA, Michael D. Diodato, MD, Yosuke Ishii, MD, Anson M. Lee, BA, Sandip M. Prasad, BA, Jegan Gopal, BA, Richard B. Schuessler, PhD, Ralph J. Damiano, Jr, MD *

Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri

Accepted for publication June 10, 2005.

* Address correspondence to Dr Damiano, Division of Cardiothoracic Surgery, Washington University School of Medicine, 660 S Euclid Ave, Box 8234, St. Louis, MO 63110 (Email: damianor{at}wustl.edu).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Microwave ablation has been used to replace the traditional incisions used in the surgical treatment of atrial fibrillation. However, dose–response curves have not been established in surgically relevant models. The purpose of this study was to develop dose–response curves for the Flex 10 (Guidant, Inc) microwave device in both the acute cardioplegia-arrested heart and on the beating heart.

METHODS: Twelve domestic pigs (40 to 45 kg) were subjected to microwave ablation in either the arrested (n = 6) or beating heart (n = 6). The cardioplegia-arrested heart was maintained at 10° to 15°C while six atrial endocardial and seven right ventricular epicardial lesions were created in each animal. On the beating heart, six right atrial and seven ventricular epicardial lesions were created. Ablations were performed for 15, 30, 45, 60, 90, 120, and 150 seconds (65 W, 2.45 GHz). The tissue was stained with 2,3,5-triphenyl-tetrazolium chloride, and sectioned at 5-mm intervals. Lesion depth and width were determined from digital micrographs.

RESULTS: Mean atrial wall thickness was 2.8 mm (range, 1 to 8 mm). In the arrested heart, 94% of atrial lesions were transmural at 45 seconds and 100% were transmural at 90 seconds. In the beating heart, only 20% of atrial lesions were transmural despite prolonged ablation times (90 seconds). Ventricular lesion width and depth increased with duration of application, and were similar on the arrested and beating hearts.

CONCLUSIONS: Microwave ablation produces linear dose–response curves. Transmural lesions can be reliably produced on the arrested heart, but not consistently on the beating heart.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
The long-term efficacy of the Cox-Maze procedure has been well established with success rates in excess of 90% [1–4]. Multiple groups around the world have attempted to simplify the procedure using various energy sources to replace the myriad of surgical incisions of the Cox-Maze procedure. These have included microwave energy, unipolar and bipolar radiofrequency energy, cryoablation, laser energy, and, more recently, ultrasound [5–9]. Early results with these new energy sources have been encouraging when used for endocardial ablation in the cardioplegia-arrested heart. This has spurred the interest in the development of a minimally invasive procedure. The goal of these efforts has been to develop an effective procedure that could be performed without cardiopulmonary bypass, on the beating heart.

There are a number of obstacles that must be overcome for these new procedures to be as successful as the traditional cut and sew Cox-Maze procedure. The most important requirement is that the device must be able to produce transmural lesions on the arrested and beating heart safely without producing collateral damage to vital structures. This requires the development of dose–response curves on living tissue that would allow surgeons to deliver appropriate energy based on the tissue depth, temperature, and the clinical situation. The purpose of this study was to investigate the FLEX 10 microwave device (Guidant, Inc, Santa Clara, CA) and to establish dosimetry in a surgically relevant model.

Microwave energy generates heat within tissue by inducing oscillation of dielectric molecules such as water [10]. The kinetic energy produced in these molecules by the microwave field is imparted to the tissue as heat. This form of heat production is known as dielectric heating. The depth of the microwave lesions is dependent on the power, the duration of application, and the type of microwave antennae [11]. The advantage of microwave over radiofrequency energy is that it produces a deeper lesion with even penetration and less surface heating [12]. Tissue temperatures exceed 50°C but remain below 100°C, hence reducing the risk of tissue charring and possible thromboembolism [13, 14].

In this study, the FLEX 10 device was used to produce endocardial atrial and epicardial right ventricular lesions on the cardioplegia- arrested heart and epicardial atrial and right ventricular lesions on the beating heart. The FLEX 10 device consists of a 26-mm antenna, which is encased in a flexible whiplike 53.5-cm polytetrafluoroethylene (Teflon) sheath (Fig 1). The antenna can be adjusted within the sheath to produce ablation lines 2 cm in length per application and a maximum ablatable segment length of 20 cm (10 x 2 cm segments) if the device is held in one position. The device principally was introduced for epicardial application on the beating heart. The manufacturer's recommended setting is 65 W for 90 seconds at a frequency of 2.45 GHz for the beating heart and 45 seconds for the arrested heart [14].



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  		Fig 1. The FLEX 10 microwave device (Guidant, Inc, Santa Clara, CA).

 

   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Experimental Protocol
Twelve domestic pigs weighing 40 to 45kg were used in this study. 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 Publications 85-23, Revised 1985). Each animal was premedicated, intubated, anesthetized, and monitored continuously throughout the procedure. The heart was exposed through a median sternotomy. In 6 animals, a cardioplegia cannula was placed in the proximal ascending aorta. The superior vena cava and the inferior vena cava were snared with umbilical tapes, and the aorta was cross-clamped. Cardioplegia solution (Plegisol; Abbott Laboratories, North Chicago, IL) was infused at a volume of 10 mg/kg and an aortic root pressure of 70 to 80 mm Hg. A myocardial temperature probe was placed into the left ventricle, and normal saline slush solution was placed topically on the heart. Cardioplegia was applied at regular intervals every 20 minutes to maintain cardiac arrest and myocardial temperature between 10° and 15°C. Right atrial and ventricular lesions were created using the FLEX 10 device. The right atrial lesions were created endocardially at 65 W and durations of 15, 30, 45, 60, 90, and 120 seconds. Right ventricular ablations were also made epicardially at 65 W and durations of 15, 30, 45, 60, 90, 120, and 150 seconds.

In 6 other animals, epicardial atrial and ventricular lesions were created on the beating normothermic heart at 65 W. Atrial lesions were performed at 15, 30, 45, 60, 90, and 120 seconds whereas right ventricular lesions were performed at 15, 30, 45, 60, 90, 120, and 150 seconds.

Histologic Assessment
At the end of the procedure, 1% 2,3,5-triphenyl-tetrazolium chloride was perfused into the left ventricle of the beating heart and into the aortic root of the arrested heart before the animals were sacrificed. The hearts were then removed en bloc. The myocardial lesions were examined for evidence of charring and tissue disruption. The hearts were then placed in 1% 2,3,5-triphenyl-tetrazolium chloride solution and incubated at room temperature for 45 minutes. Each microwave lesion was sectioned four times, 5.0 mm apart, perpendicular to the long axis of the ablation line. Each section was then digitally photographed along with a 5-mm caliper to allow for calibration (Fig 2). Lesion width and depth and atrial tissue thickness were analyzed using commercial software (Adobe Photoshop, San Jose, CA). The lesion depth and width were measured from the unstained area to the pink halo region surrounding each lesion. The accuracy of this technique was ± 0.03 mm. A total of 13 lesions from each animal were examined.



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  		Fig 2. The right ventricular ablations were sliced every 5 mm for measurement of lesion width and depth.

 
Statistical Analysis
Data were compared with repeated-measures analysis of variance with one factor. Data were expressed as mean ± standard deviation and considered significant with p less than 0.05.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
On gross inspection, the lesions were pale and easily visible. No tissue disruption was observed. Tissue charring was minimal and occurred principally at ablation times greater than 90 seconds. Atrial lesion depth was compared with atrial wall thickness in the area of ablation, and the number of transmural lesions was determined. The mean atrial tissue thickness was 2.88 ± 0.4 mm with a range of 1 to 8 mm.

Atrial Ablation on the Arrested Heart
Ninety-four percent of ablated atrial sections created on the arrested heart were transmural at 45 seconds (n = 16) and 100% of ablated atrial sections were transmural at 90 seconds (n = 14; Fig 3). In some instances, the ablation lines produced on the atrium were less than 4 cm in length even though two continuous 2-cm segments of the device were activated. All sections of every tissue sample were transmural after 90 and 120 seconds of ablation for the arrested heart.



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  		Fig 3. Percent transmural lesions (%) versus duration of ablation in the cardioplegia-arrested heart.

 
Atrial Ablation on the Beating Heart
The data on the beating heart showed a distinctly different profile (Fig 4). Overall, 20% of atrial lesions were transmural in the beating heart. There was no relationship between time of ablation and lesion transmurality.



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  		Fig 4. Percent transmural lesions (%) versus duration of ablation in the beating heart.

 
Ventricular Dosimetric Curves
Dosimetric curves were established for the FLEX 10 device from right ventricular ablations on the cardioplegia-arrested heart and the beating heart. These curves were established on ventricular tissue because atrial tissue was too thin to allow for the accurate determination of the dose–response relationship. The average right ventricular wall thickness was 8.2 ± 2.9 mm with a range of 3.2 to 17.6 mm. Lesion depth and width increased with duration of ablation for FLEX 10 device. Ventricular lesion depth ranged from 0.5 mm (45 seconds) to 9.5 mm (150 seconds) on the arrested heart and from 1.1 mm (45 seconds) to 11.9 mm (150 seconds) on the beating heart. The relationship of mean ventricular lesion depth versus time was similar for the arrested and beating heart (Fig 5). The mean lesion depth for the FLEX 10 device at 90 seconds (65 W) was 4.1 ± 1.3 mm on the arrested heart and 4.6 ± 1.3 mm on the beating heart (p = 0.751).



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  		Fig 5. Ventricular lesion depth versus duration of ablation in both the cardioplegia-arrested (squares; broken line) and the beating heart (diamonds; solid line). Data are expressed as mean ± standard deviation.

 
Lesion width for the FLEX 10 device ranged from 2.1 mm (45 seconds) to 12.6 mm (150 seconds) on the arrested heart and 2.6 mm (45 seconds) to 13.6 mm (150 seconds) on the beating heart. As opposed to lesion depth, lesion width was wider on the beating heart compared with the arrested heart (p < 0.001; Fig 6).



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  		Fig 6. Ventricular lesion width versus duration of ablation in both the cardioplegia-arrested (squares; broken line) and the beating heart (diamonds; solid line). Data are expressed as mean ± standard deviation.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Microwave ablation has been widely used for the surgical treatment of atrial fibrillation [15–17]. Good results have been obtained both on the arrested heart and the beating heart [18, 19]. Although the energy has proven to be safe, there have been isolated reports of collateral tissue injury [20]. Despite this clinical experience, there have been no published dose–response curves for this technology on living myocardial tissue under surgically relevant conditions. This information is imperative for effective and safe use of this energy on atrial myocardium. It will allow surgeons to rationally select ablation times and hopefully avoid complications.

This study demonstrated that the FLEX 10 device was capable of producing transmural atrial lesions on the cardioplegia-arrested heart. The lesions were well defined and easily visible. All atrial lesions created on the arrested heart were transmural with ablation duration of 90 seconds. The lesions that did not achieve transmurality were over the trabeculated areas of the right atrium, particularly the crista terminalis, which can achieve thicknesses up to 8 mm. However, our dose–response curves suggested that more prolonged ablation will be required in patients if atrial thickness exceeds 4 mm, as may be the case in the human diseased atria. In this study in a porcine model, the mean atrial thickness was less than 3 mm.

On the beating heart, it was difficult to produce transmural lesions consistently. Only 20% of ablated atrial sections were transmural even with prolonged ablation times. Interestingly, the mean lesion depth did not increase significantly with time. At 45 seconds, mean lesion depth was 2.3 ± 0.8 mm and at 120 seconds mean lesion depth was 2.6 ± 1.0 mm. The circulating blood pool with its cooling effect on the endocardium is likely responsible for this limitation on lesion depth. Epicardial fat also may have restricted the depth of some lesions. These findings should cause surgeons to cautiously use this technology in this setting because of its inability to create transmural lesions.

Other investigators have documented similar difficulty in creating transmural lesions on the beating heart with both microwave and other unipolar energy sources, particularly radiofrequency energy. Van Brakel and colleagues [21] experienced limited success with the FLEX 10 device in creating transmural lesions on the beating heart. In their study, 33% ± 19% of the lesions created on the beating heart acutely were transmural. However, the percentage of transmurality increased in the chronic setting to 66% ± 14% [21]. A similar shortcoming was demonstrated with unipolar radiofrequency ablation on the beating and arrested heart in an ovine model. Epicardial fat and the circulating blood pool were believed to have an important negative effect on the production of transmural lesions [22]. Our laboratory found unipolar radiofrequency to be incapable of creating transmural lesions in an ovine beating heart model [23]. In humans, only 8% of lesions created on the beating heart with unipolar radiofrequency were transmural [24].

There has been controversy in the literature as to whether the creation of transmural lesions is necessary to surgically cure atrial fibrillation. However, it is not arguable that lesions must create conduction block to be effective as a treatment for atrial fibrillation [25]. Ablation lines are designed to either electrically isolate the triggers in the pulmonary veins or block the macro-reentrant circuits responsible for permanent atrial fibrillation. Unfortunately, the only guarantee of complete and permanent conduction block is a transmural lesion. Thus, our data would suggest that microwave ablation should be used with caution on the beating heart unless pacing can be used to document conduction block. During pulmonary vein isolation, pacing to establish conduction block can be used as an indicator of adequate lesion depth. However, there is no such indicator for transmurality for other lesions used in the Cox-Maze or other procedures for atrial fibrillation.

The dose–response curves yielded clinically relevant information about the biophysics of microwave ablation on living tissue. The importance of recognizing the dosimetry of this device cannot be overemphasized if the surgeon is to avoid injury to collateral structures. Interestingly, there was no significant difference in lesion depth between the two groups, and the dosimetry curves for both the beating and the arrested heart were similar. These data suggest that in thick ventricular tissue there is little effect of the circulating blood volume on lesion depth. The lesion depth increased with duration of ablation and exceeded a depth of 4 mm after 90 seconds of ablation in both the cardioplegia-arrested and beating heart. Although normal atrial thickness is less than 5 mm, the myocardium may be thicker in the region of the crista terminalis and in diseased atria [22]. However, the FLEX 10 device was capable of producing lesions in excess of 6 mm at extended periods of ablation in both the cardioplegia-arrested heart and the beating heart. It would appear that the ability of microwave energy to penetrate the ventricular tissue was unaffected by the tissue temperature. In contradistinction, it was observed that the lesions created on the right ventricle were significantly wider in the beating heart when compared with the arrested heart. This difference in lesion width may have been related to the lower baseline temperature of the arrested heart. In the arrested heart, the myocardial temperature was maintained at 10° to 15°C as compared with 37°C for beating heart procedures.

Study Limitations
The main limitation of this study was that it was performed in an acute model. It is possible that a chronic model would have yielded slightly different results, in that there may be lesion extension with time [21]. However, 2,3,5-triphenyl-tetrazolium chloride staining has been documented to be effective, reliable, and sensitive in determining the extent of necrosis [26]. Our laboratory has used this previously, and has found that acute results with 2,3,5-triphenyl-tetrazolium chloride staining correlated well with chronic histologic examination [27, 28].

The second limitation of this study was that it examined the effect of microwave ablation on normal porcine hearts. It is possible that results would differ under pathologic states. Usually, atrial thickness is increased in patients with valvular heart disease. This would exacerbate any difficulties seen with transmurality. Another unavoidable shortcoming of this study was that dose–response curves were determined on right ventricular tissue. Unfortunately, atrial tissue is too thin to allow for accurate determination of dosimetry. However, there is no reason to expect that there would be significant biophysical differences between atrial and ventricular microwave ablation. Finally, the method used for determining lesion depth and width, although accurate, can be prone to observer error. A caliper set at 5 mm was always photographed along with the tissue sample, and this was used as a reference of measurement in an attempt to reduce error.

Conclusions
Dose–response curves for the FLEX 10 device were established in the cardioplegia-arrested heart and on the beating heart. In myocardial tissue unaffected by the cooling effects of the circulating blood volume, the device was capable of producing lesions in excess of 4 mm in depth both on the cardioplegia-arrested and on the beating heart. However, the device failed to create transmural atrial lesions consistently on the beating heart. It is recommended that surgeons should avoid using this device for beating heart pulmonary vein isolation or at least incorporate pacing after the procedure to confirm conduction block.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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