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Ann Thorac Surg 1999;67:666-671
© 1999 The Society of Thoracic Surgeons

Original Articles

Experimental application of microwave tissue coagulation to ventricular myocardium

Hiroshi Watanabe, MDa, Jun-ichi Hayashi, MDa, Masaaki Sugawara, MDa, Masahide Hiratsuka, MDa, Shoji Eguchi, MDa

a Department of Thoracic and Cardiovascular Surgery, Niigata University School of Medicine, Niigata, Japan

Accepted for publication August 10, 1998.

Address reprint requests to Dr Watanabe, Department of Thoracic and Cardiovascular Surgery, Niigata University School of Medicine, 757 Asahimachi-dohri 1, Niigata City 951-8510, Japan
e-mail: watanabe{at}med.niigata-u.ac.jp


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. It is difficult to create transmural lesions in a beating, normothermic perfused heart. The aim of this study was to evaluate the effect of microwave tissue coagulation on a beating heart.

Methods. We used a microwave tissue coagulator that emits microwaves of 2,450 MHz. Studies were conducted on 30 mongrel dogs weighing between 9 and 13 kg, and microwave tissue coagulation was performed at the free wall of the left ventricle in a beating heart without cardiopulmonary bypass.

Results. Microwave tissue coagulation created transmural degenerated lesions in the left ventricle without risk of ventricular rupture. The lesion width of microwave ablation increased from 10 to 60 seconds. Histologic examinations revealed well-demarcated areas of heat degeneration consisting of coagulation necrosis and contraction band necrosis of the myocardium. The lesion healed to hard scar tissue, which was sharply demarcated from the normal myocardium. No animals had inducible ventricular tachycardia through programmed ventricular stimulation.

Conclusions. Microwave ablation with a monopolar antenna created transmural lesions with only a few proarrhythmic events occurring during ablation.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Catheter ablation and surgical ablation have become effective therapeutic tools for treatment of drug refractory, life-threatening arrhythmias. Surgical treatment for arrhythmia is based on isolation or ablation of arrhythmogenic foci or reentry circuits. Cryothermia has been widely accepted as a safe and effective method for surgical ablation at many institutions [1–5]. Recently, laser ablation has been introduced into clinical use [6–8]. However, the creation of cryolesions can be time-consuming, and cryolesion depth is affected by tissue temperature [5], making it difficult to create transmural lesions in a beating, normothermic perfused heart because the warm blood flow in the myocardium attenuates the cryothermic effect. Although laser ablation can create thermal lesions in normothermic myocardium, the width and depth of coagulated myocardium are affected by myocardial color, tissue construction, irradiation method, and many other factors [9], and it is difficult to create a constant volume of laser lesion. Radiofrequency catheter ablation has been accepted as a safe and effective therapeutic tool [10–12]. However, maximal depth of the lesion produced by radiofrequency energy at 20 to 50 W is 5 mm [13].

Microwave tissue coagulation creates thermal injury through a radiated electromagnetic field and creates a lesion in the normothermic, beating heart [14]. The depth of the coagulated lesion depends on the design of the antenna, particularly the length of inner conductor [15]. However, few data are available regarding the characteristics of microwave ablation of the myocardium and the response of the myocardium to microwave hyperthermic exposure [14, 16, 17]. The purposes of the present study were to explore short- and long-term histologic changes, the possibility of cardiac rupture, and arrhythmogenicity after microwave coagulation.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Animal preparation
Thirty mongrel dogs weighing between 9 and 13 kg were anesthetized with sodium pentobarbital (30 mg/kg). Their lungs were ventilated with a Harvard respirator. A surface electrocardiogram was monitored continuously. A left lateral thoracotomy was performed at the fifth intercostal space, and the pericardium was opened to expose the heart. All animals received humane care in compliance with the "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research and the "Guide for the Care and Use of Laboratory Animals" prepared by the National Institutes of Health (NIH Publication no. 86-23, revised 1985).

Lesion generation
Microwave lesions were created with a 2,450-MHz microwave generator (OT-110M; Heiwa Electronic Ind, Ltd, Shijonawate, Osaka, Japan). Microwave energy was applied to the ventricular myocardium by a monopolar antenna (Fig 1). The antenna consisted of an inner conductor (0.7 mm in diameter and 1 cm in length) that protruded beyond the outer conductor. The inner conductor was inserted toward the free wall of the left ventricle until the outer conductor touched the epicardial surface. In the experiments on the acute effects of microwave tissue coagulation (22 dogs), microwave energy was delivered at 30 or 50 W, for 10, 20, 30, or 60 seconds for each lesion. We created 5 or 6 lesions at each power setting, and the total number of created lesions was 44 (1 to 8 lesions per heart). In the experiments on the long-term effects (eight dogs), we chose a power setting of 50 W for 30 seconds.



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  		Fig 1. Monopolar antenna used for microwave ablation.

 
Electrophysiologic study
After creation of the microwave lesions, an electrophysiologic study was performed as a provocative test for ventricular arrhythmias. We inserted temporary pacemaker wires on the apex and the anterior surface of the right ventricle. Stimuli were given at twice the late diastolic threshold and of 2-msec duration by a programmable cardiac stimulator. One or two extra stimuli were delivered after eight basic stimuli (300 msec) at the apex or in the outflow tract of the right ventricle. Isoproterenol was not used in the present study.

Determination of lesion size
After application of microwaves with varying doses of energy, 22 dogs were sacrificed to study the short-term effects of microwave ablation. The hearts were fixed in 10% formalin and subjected to gross and microscopic examination. Each lesion was carefully sectioned through its center, and maximum widths and depths were measured.

Collection of hearts
To study the long-term effects of microwave tissue coagulation, eight dogs were anesthetized with sodium pentobarbital and sacrificed at 1, 3, 7, and 14 days and 1, 3, 6, and 12 months after microwave ablation.

Histologic study
After fixation with 10% formalin, the myocardial tissue was stained with hematoxylin-eosin and then assessed by light microscopy.

Statistical analysis
Results were expressed as mean ± standard deviation. Statistical analysis was performed using Student’s t test. Differences were considered to be significant if probability values were less than 0.05.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
No deaths occurred during operation and among the eight long-term survivors.

Electrocardiographic and electrophysiologic studies
During application of microwave energy to the ventricular myocardium, all dogs developed premature ventricular contractions (Fig 2). However, few ventricular arrhythmias were observed after ablation in short-term and long-term follow up. After creation of the microwave lesion, programmed ventricular stimulation did not induce ventricular tachycardia in any of the dogs at any time.



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  		Fig 2. Representative electrocardiogram during microwave ablation. Premature ventricular contractions and nonsustained ventricular tachycardia occurred during ablation.

 
Histologic examination
In the study of short-term effects, the gross appearance of the ventricular myocardium fixed with 10% formalin demonstrated an elliptic, slightly dented, and well-demarcated area of thermal injury. Tissue defects were found at the site of antenna insertion, but no bleeding or burning of the myocardial surface was found. A horizontal section through a tissue lesion induced by microwave energy was oval shaped, and the maximum lesion width of the intramural level was greater than that of the epicardial surface (Fig 3). A border zone between the necrotic myocardium and the normal myocardium consisted of myocardial edema and an intramural hemorrhage. Microwave tissue coagulation created transmural lesions independent of microwave energy level and duration of ablation. No fresh thrombus was recognized over the coagulated endocardial surface. No rupture of the heart was caused by microwave ablation.



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  		Fig 3. Heart fixed with 10% formalin. (A) The lesions were created by application of microwave energy at 50 W for 30 seconds. (B) Horizontal section through a tissue lesion.

 
Light microscopy revealed coagulation necrosis in the center of the lesion and contraction band necrosis in the border zone. Marked interstitial edema and hemorrhage were recognized throughout the lesion (Fig 4).



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  		Fig 4. Light microscopic findings after microwave tissue coagulation (hematoxylin-eosin stain). (A) Created lesion reached the endocardial surface (original magnification x5). (B) Coagulation necrosis in the center of the lesion and (C) contraction band necrosis in the border zone (original magnification x50).

 
Lesion size
Figure 5 depicts the relation between the coagulation time and the lesion size in the left ventricular myocardium. The lesion width of microwave ablation increased from 10 to 60 seconds at either 30 or 50 W (6.00 ± 0.63, 6.60 ± 0.49, 10.83 ± 1.77, and 13.00 ± 1.67 mm at 30 W for 10, 20, 30, and 60 seconds, respectively; 5.83 ± 0.69, 9.40 ± 1.96, 11.83 ± 1.46, and 15.83 ± 0.69 mm at 50 W for 10, 20, 30, and 60 seconds, respectively). However, neither microwave energy power nor coagulation time affected the lesion depth, and all lesions were transmural (10.60 ± 3.07, 10.40 ± 1.02, 11.83 ± 2.27, and 12.60 ± 1.74 mm at 30 W for 10, 20, 30, and 60 seconds, respectively; 9.83 ± 0.90, 11.60 ± 1.85, 11.50 ± 2.22, and 11.50 ± 1.89 mm at 50 W for 10, 20, 30, and 60 seconds, respectively).



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  		Fig 5. Relation between the coagulation time and lesion width or lesion depth in the left ventricular myocardium.

 
Histologic examination
In the study of long-term effects, at 1 day and 2 days after microwave ablation, the necrotic muscle with intramural hemorrhage was sharply demarcated from the normal myocardium. Young granulation tissue that consisted of macrophages, lymphocytes, fibroblasts, and capillary vessels was recognized on the border zone between the ablated lesion and the normal myocardium at 1 week after microwave tissue coagulation. At 2 weeks, granulation tissue expanded from the border zone to the center of the necrosis. At 1 month, the necrosis was present only in the center of the lesion, and most of the necrotic muscle was replaced by fibrotic tissue. Healing by fibrosis was complete by 3 months and fatty tissue infiltrated a small area of the ablated lesion. After 6 months, the necrotic myocardium healed to white-colored hard scar tissue, which was sharply demarcated from the normal myocardium. Light microscopy showed that the scar tissue consisted of collagen fibers and infiltrated fatty tissue at 12 months (Fig 6). Throughout the healing process of the microwave tissue coagulation, the lesion was sharply demarcated from the normal myocardium. There was no aneurysmal change of the ablated myocardium, and no thrombus formation was recognized over the coagulated myocardial surface.



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  		Fig 6. (A) Horizontal section of the heart fixed with 10% formalin at 12 months after microwave tissue coagulation. (B) The lesion was sharply demarcated from the normal myocardium, and scar tissue consisted of collagen fibers and infiltrated fatty tissue (hematoxylin-eosin stains, original magnification x10).

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
In patients with medically refractory ventricular tachycardia, surgical treatment has proved effective. Cryothermia [1–3] and laser ablation [7, 8] have improved surgical results. It is essential for ablation of arrhythmogenic foci and reentry circuits to create a lesion sharply demarcated from normal myocardium. The ablated lesion should heal into firm scar tissue that does not spread and should be like an inert plug that has displaced a portion of myocardium with minimal disruption to the surrounding tissue. The lack of arrhythmogenicity of the chronic lesion is important for surgical therapeutic tools.

Tabuse [15] developed a microwave tissue coagulator for hepatectomy in 1979. Tabuse and colleagues [18] reported excellent clinical results using microwave ablation as a method for controlling bleeding during hepatic lobectomy. Recently, microwave tissue coagulation has been used for endoscopic treatments [19]. As a method to ablate myocardium, microwave energy has been tried for catheter ablation in experiments [14, 16, 17], but intraoperative microwave ablation has not been established. The mechanism of microwave ablation is a heat injury in which irreversible cellular electrophysiologic changes and myocardial contracture develop at hyperthermic temperatures above 50°C [14]. Heating with microwaves results from a propagating electromagnetic field that increases the energy of the dielectric molecules. While maintaining alignment with the alternating electric field, neighboring energized dipolar molecules collide with each other, producing heat primarily as a result of friction [20]. Whayne and colleagues [14] reported that the steady-state temperature at the antenna-tissue interface at 50 W for 300 seconds was 70.4 ± 13.5°C for microwave lesions, and that the tissue temperature decreased as the distance from the antenna increased. The tissue temperature heated by microwave energy does not rise over 100°C; therefore, microwave tissue coagulation carries no risk of charring or vaporization.

Histologic examination revealed coagulation necrosis in the center part of the ablated lesion and contraction band necrosis with an intramural hemorrhage in the border zone between the necrotic myocardium and the normal myocardium, which resembled laser-ablated lesions [6–8, 21]. These histologic changes were produced by heat injury. We emphasize that the depth of ablated lesions is determined by the length of the inner conductor and that inner conductor length should be chosen according to the depth of the ablated lesion needed.

Many previous studies reported the efficacy of cryothermia in experiments and clinical use [1–5]. However, it is difficult to create transmural lesions. Cryolesion depth is affected by tissue temperature and duration of application. Holman and associates [5] showed that an average lesion depth was 3.0 mm in the normothermic perfused canine heart and 8.0 mm in the hypothermic cardioplegic arrested heart (6° to 12°C) at -60°C for 120 seconds. Therefore, we apply cryothermia under hypothermic cardioplegic arrest to enhance the cryothermic effect. However, many patients with ventricular arrhythmia have low cardiac function and it is desirable to avoid aortic cross-clamping to prevent severe postoperative cardiac failure. Hyperthermic ablation methods such as laser ablation have the advantage of ablation in the normothermic beating heart.

Laser ablation has been proved to create lesions in normothermic myocardium [6–8]. However, laser ablation involves the risk of charring and crater formation, leading to tissue perforation in the center part of the irradiated area as the amount of laser energy increases [6]. Therefore, continuous monitoring of myocardial temperature with a needle thermometer and cooling the irradiated myocardium with 0°C saline are recommended [22]. Because laser energy absorbed by the myocardium is affected by its color, coagulated volume in the red myocardium (beating heart) differs from that in the white myocardium (cardioplegic arrested heart) [9]. Microwave coagulation does not need myocardial temperature monitored nor cooling the myocardium to prevent charring or vaporization, and the depth of the ablated lesion is determined by the length of the inner conductor.

Radiofrequency catheter ablation has been accepted as a safe and effective therapeutic tool [10–12]. Maximal depth of the lesion produced by radiofrequency energy at 20 to 50 watts is 5 mm [13]. Therefore, it is difficult to create transmural lesions using the radiofrequency catheter ablation technique. Ohtake and associates [23] recently developed an intraoperative radiofrequency ablation technique using a needle electrode. They used 0.25-MHz radiofrequency with an output power of 3 W and durations from 3 to 15 seconds. In this setting, the ablated lesion was 3.18 ± 0.3 mm in width and 7.05 ± 0.3 mm in depth, using a 3-mm-long needle electrode. Because of the small amount of energy they used, the possibility of creating transmural lesions is not known. In addition, radiofrequency energy is delivered between the electrode applied to the heart and the external neutral electrode. The body tissue between the electrodes is exposed to radiofrequency energy during ablation. In contrast, microwave ablation does not need the external neutral electrode, and the body tissue, except the myocardial region where the electrode is applied, is not exposed to microwave energy. The electromagnetic field propagated by microwave is limited around the antenna, and the lesion depth is determined by the length of inner conductor [15].

In the present study, we found that microwave ablation with a monopolar antenna can produce transmural lesions with no risk of perforating the heart. However during microwave ablation, premature ventricular contractions occurred in all dogs, although no arrhythmia was observed after ablation. Therefore, in patients who have ventricular arrhythmia induced by programmed electrical stimulation, surgeons must pay close attention to the induction of ventricular tachycardia or ventricular fibrillation induced by premature ventricular beating during microwave ablation. In addition, it would be desirable to apply microwave energy to the myocardium under cardiopulmonary bypass support in high-risk patients. The limitations of this study were absence of contiguous lesions, limitation to left ventricular myocardium, and single lesions in single animals at each time point.

In summary, we demonstrated that microwave ablation with a monopolar antenna created transmural lesions with only a few proarrhythmic events occurring during ablation. These results suggest that microwave ablation can be useful in the treatment of tachyarrhythmias from deep foci of ventricular myocardium.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
We thank Hisaichi Higuchi for his technical assistance. This study was supported by a Grant-in Aid for Scientific Research C (No. 04670819) in Japan.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

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  12. Klein L.S., Shih H.T., Hackett F.K., Zipes D.P., Miles W.M. Radiofrequency catheter ablation of ventricular tachycardia in patients without structural heart disease. Circulation 1992;85:1666-1674.[Abstract/Free Full Text]
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