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Ann Thorac Surg 2004;78:1397-1402
© 2004 The Society of Thoracic Surgeons

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Original article: cardiovascular

Evaluation of Epicardial Microwave Ablation Lesions: Histology Versus Electrophysiology

^a Departments of Cardiothoracic Surgery and Physiology, Cardiovascular Research Institute Maastricht, Maastricht, the Netherlands, Department of Surgery and the Center for Minimally Invasive and Robotic Surgery, and Department of Comparative Medicine, Brody School of Medicine, East Carolina University, Greenville, North Carolina

Accepted for publication April 1, 2004.

^* Address reprint requests to Dr van Brakel, Department of Cardiothoracic Surgery, Cardiovascular Research Institute Maastricht, University Hospital Maastricht, P. Debyelaan 25, Postbus 5800, 6202 AZ Maastricht, the Netherlands
t.vanbrakel{at}ctc.unimaas.nl

Presented at the Fortieth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 26–28, 2004.

	Abstract

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
BACKGROUND: Pulmonary vein isolation is a hallmark in current surgical ablation for atrial fibrillation. However, validation of isolation remains cumbersome. We evaluated electrophysiologic and not histologic means to test isolation.

METHODS: In 16 mongrel dogs, robot-assisted epicardial beating-heart microwave ablation (FLEX 10) was performed around the pulmonary veins. Electrophysiologic isolation was tested by pacing at 4 times threshold values inside and outside the pulmonary veins (exit and entrance block). The histology of lesions was studied for transmurality and continuity of the lesion lines. In 5 dogs, lesions were studied at various time intervals.

RESULTS: Histologic evaluation of the lesions showed incomplete (48% ± 20%) circumferential myocardial damage in all dogs with acute lesions. Electrophysiologic evaluation showed completion of the box (entrance and exit block) in 8 dogs and in another 5 dogs after repeated ablation (p < 0.01 compared with histologic evaluation). Electrophysiologic evaluation of the dogs with chronic lesions showed completed lesions in 4 of 5 dogs directly after ablation. At follow-up (1 to 3 weeks), the isolations remained electrophysiologically complete. Histologic evaluation of the lesions 1 to 3 weeks after ablation showed complete (100%) circumferential lesions in all 4 dogs (p < 0.001 compared with the histology of dogs with acute lesions).

CONCLUSIONS: Directly after treatment, ablation lesions are best evaluated electrophysiologically, because complete (transmural and circumferential) lesions are not shown by histologic evaluation in the acute stage. After 1 to 3 weeks, the histology is in accordance with the electrophysiology. To obtain a complete isolation, online electrophysiologic evaluation during pulmonary vein microwave ablation is necessary to optimize the results.

	Introduction

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
The evidence that ectopic foci originating from the pulmonary veins play an important role in the initiation and maintenance of atrial fibrillation (AF) [1, 2] has accelerated the development of surgical treatment of AF toward a simplification of the procedure by a minimized lesion pattern that includes isolation of the pulmonary veins. Recently, minimally invasive techniques have been developed that use epicardial beating-heart ablation to further optimize the surgical treatment of AF [3–6]. Beating-heart epicardial ablation, however, cannot be compared with arrested heart endocardial ablation, because blood cooling and epicardial fat can effect the catheter potency to produce transmural lesions. Therefore, both experimental and clinical evaluation of the epicardial ablation lesions are of great importance. Because transmural and continuous lesions are believed to be essential for effective ablation lines, most surgical studies have concentrated on histologic evaluation of the lesions. Especially epicardial ablation, but also endocardial ablation, showed incomplete tissue damage in a number of studies [7–9]. Validation of ablation lesions in terms of electrophysiologic evaluation has been studied intensively by electrophysiologists using various pacing and mapping techniques, but electrophysiologic findings were mostly not related to the transmurality and continuity of the ablation lesions [10, 11]. Hence, it remains unclear whether histologic incomplete lesions are also ineffective in terms of blocking atrial conduction.

The purpose of this study was to compare histologic and electrophysiologic evaluation of a beating-heart epicardial microwave ablation lesion encircling the pulmonary veins. We also addressed the question of whether the efficacy of these evaluation methods differs between acute and evolving lesions.

	Material and Methods

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
Epicardial Beating-Heart Pulmonary Vein Microwave Ablation
Sixteen mongrel dogs weighing 18 to 27 kg (23 ± 3 kg) were used in this study. Eleven dogs were used for acute lesion evaluation, whereas in 5 dogs lesions were evaluated after 1 to 3 weeks. All animals received humane care in compliance with the Guide for the Care and Use of Laboratory Animals (National Institutes of Health Publication 86-23, 1985 revision). Experiments were approved by the University Animal Care and Use Committee at East Carolina University. Dogs were anesthetized with 22 mg/kg sodium pentobarbital intravenously and were maintained on isoflurane (1% to 3%) with a 1:2 mixture of oxygen and nitrogen by using a positive pressure ventilator (MDS Matrx, Orchard Park, NY). Arterial invasive blood pressure, electrocardiogram, and oxygen saturation (pulse oximeter) were monitored throughout the experiment.

A 4-cm right minithoracotomy incision was made in the fourth intercostal space. The pericardium was incised to expose the right and left atria. Six electrodes were placed on the atria: 2 inside the pulmonary vein, 2 on the left atrium outside the pulmonary vein area, and 2 on the right atrium. Electrodes were made from 2 silver buttons (diameter, 1.5 mm; distance, 5 mm) embedded in silicone for bipolar recording and pacing. The electrode patches were sutured to the epicardial surface of the atria by a single U-shaped stitch (Prolene 5-0; Ethicon, Somerville, NJ). After electrode placement, 2 robotic arms and the robotic camera were introduced (da Vinci robotic system; Intuitive Surgical, Sunnyvale, CA). Pulmonary veins were circumferentially dissected. The microwave ablation catheter (FLEX 10; Afx Inc, Fremont, CA) was introduced with robot assistance and passed in a lassolike fashion around all pulmonary veins. The ablation was performed sequentially (2 cm per ablation; 65 W; 90 seconds) until an encircling box lesion was obtained. Figure 1 shows a sketch of the atria depicting the placement of the electrodes and the box lesion around the pulmonary veins.

View larger version (26K): [in this window] [in a new window]   Fig 1. Schematic view of the left and right atrium (LA and RA) with the pulmonary veins (PV's) and the superior and inferior caval veins (SVC and IVC). The gray stars indicate the placement of the pacing and sensing electrodes. The arrow indicates the atrial septum. The ablation lesion around the PVs is presented by the thick circle.

Histologic Evaluation of Lesions
All dogs with acute lesions were killed, and the heart and part of the lungs were taken out to ensure proper dissection of the ablation line. Affected atria were dissected immediately after death by excising the ablation line around the atria. The atria were inspected macroscopically for thrombus formation, endocardial tissue damage, and pulmonary vein stenosis. The atria, including the lesion, were then fixed in 10% neutral buffered formalin. After fixation, the lesion was sectioned in the plane of the lesion by using the epicardial visual damage to ensure that the lesion was cut through the middle. Tissues were paraffin-embedded and then trimmed to 5-µm sections. The sections were stained with hematoxylin and eosin as well as Gomori's trichrome.

Histologically, samples were evaluated for the following variables: percentage of viable myocardium, as evidenced by red staining on Gomori's trichrome; percentage of transmurality of lesions; percentage of circumferentiality of lesions at all layers of the atrial wall; hemorrhage; myocardial edema; myocyte necrosis; myocyte regeneration; and degree of fibrosis. The percentage of transmurality and circumferentiality of the lesions were calculated by the area of nonviable myocardium divided by the total calculated area of myocardium. The remaining variables were evaluated on a semiquantitative scoring system (0, none; 1, minimal; 2, mild; 3, moderate; and 4, severe).

Chronic Experiments
Operative and electrophysiologic measurements were performed as described previously but under sterile conditions. Five dogs underwent ablation, and lesions were electrophysiologically evaluated during ablation. One to 3 weeks after initial ablation, the dogs were anesthetized (as described previously), and a thoracotomy was performed to expose the heart for electrode placement inside the box and on the right and left atrium. Exit and entrance block were evaluated. After scarification, the heart was harvested for histologic analysis as described previously.

Statistics
Data are reported as mean ± standard deviation. Histologic comparisons of the acute and chronic data, as well as comparisons of the electrophysiologic and histologic evaluation, were performed with Student's t test. Differences were considered statistically significant if the p value was less than 0.05.

	Results

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
Electrophysiologic Evaluation
Entrance and exit block by pacing from outside and inside the box was obtained in 8 dogs (50%). After repeated ablation, complete isolation was obtained in another 4 dogs and in a fifth dog after a third ablation procedure. This increased the total success percentage from 50% to 81% compared with the first ablation (from 8 to 13 dogs). A typical example of exit and entrance block measured during ablation is shown in Figure 2. In 3 dogs, complete isolation could not be achieved after 2 to 3 ablation procedures. No differences were observed between online measurements and measurements after 1 hour. The pacing thresholds during control measurements for electrodes inside (1.5 ± 1 mA) and outside (1 ± 0.5 mA) the box did not change after complete isolation (1.5 ± 1 mA and 2 ± 1.5 mA, respectively). Pacing after complete isolation was performed with increasing thresholds with a mean box entrance threshold of 24.8 mA (range, 18.5 to 25.5 mA) and a mean box exit threshold of 23.8 mA (range, 18 to 25.5 mA).

View larger version (16K): [in this window] [in a new window]   Fig 2. The upper panel shows a typical example of online pacing from the pulmonary veins (PV) with conduction to the right atrium (RA) and left atrium (LA). The middle panel depicts pacing from the PV with capture inside the box without conduction to the RA and LA. The lower panel shows confirmation of entrance block in the same box lesion by pacing from the right atrium without capture inside the box. (I = electrocardiogram lead I.)

Histologic Evaluation
Microscopic evaluation of the acute lesions showed myocyte necrosis and heat changes in all layers of the heart. Lesions showed large areas of coagulation necrosis, contraction bands, hemorrhage, and intramyocardial edema. However, multifocal islands of normal myocardium were present within the area of ablation. None of the dogs with acute lesions showed complete transmural and circumferential damage. The estimated percentage of transmurality and complete circumferentiality per lesion is shown in Table 1. Lesion circumferentiality was graded on the epicardial surface because circumferential damage did not extend through all 3 layers of the myocardium in all lesions. Figure 3 shows a representative atrial cross section with discontinuous and multifocally transmural myocardial tissue damage in a dog with a complete electrophysiologic closed box lesion. Please note the multiple foci of pink-staining (viable) cardiomyocytes surrounded by blue-staining cardiomyocytes (degenerate/necrotic myocytes).

View larger version (53K): [in this window] [in a new window]   Fig 3. (Left) Macroscopic view of a circumferential section though the ablation lesion, showing normal myocytes red and degenerate or dead myocytes blue (stained with Gomori's trichrome). (Right) The plane of the section (B) through the lesion (A).

View larger version (158K): [in this window] [in a new window]   Fig 4. Microscopic image of subendothelial fibrosis. (Hematoxylin & eosin, x10.) This section is from a chronic lesion and shows extensive subendothelial, endocardial, and myocardial fibrosis (top three fourths of section). The adjacent myocardium varies from degenerated myocardium and from islands of normal tissue.

	Comment

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
In this study, acute and chronic epicardial ablation lesions were validated by 2 different methods: histologic and electrophysiologic evaluation. The data clearly demonstrate that there is a discrepancy between these evaluation methods and that complete lesions are best evaluated electrophysiologically rather than histologically. Electrophysiologic evaluation showed a 2-directional conduction block in 13 of the 16 lesions, whereas the histology showed nontransmurality and partial continuity in all the acute lesions. In the experiments with chronic lesions, histology was more in accordance with the electrophysiologic evaluation, because all lesions with a bidirectional conduction block showed 100% circumferential tissue damage. This indicates that acute electrophysiologic measurements are more in line with eventual electrophysiologic and histologic outcome than acute histologic assessment by itself.

Producing histologic transmural and continuous lesions is believed to be a prerequisite. That continuous and transmural lesions are difficult to obtain by epicardial ablation was also reported by Thomas and colleagues [7], who showed by using radiofrequency energy in the ovine heart that epicardial fat has an important negative effect on epicardial lesion formation. Also, clinically, in patients with mitral valve pathology and concomitant AF, it was shown that after epicardial radiofrequency ablation of the beating heart, only 3 of 38 lesions were histologically transmural [9]. Preliminary data by Melo and colleagues [12] also showed nontransmural biopsy samples from epicardial and endocardial ablation lesions. Although the current study was not conducted to investigate the cause of incomplete histologic lesions, the authors would like to stress some possible explanations. First, epicardial fat tissue may be responsible for insufficient energy delivery to the endocardial layers. Second, the highly variable wall thickness (as shown in Fig 3) suggests that not all endocardial layers received the right amount of microwave energy. Third, histologic evaluation may not be 100% sensitive for tissue damage.

The primary goal of any set of lesions is to create a conduction block to prevent atrial reentry or to isolate AF-inducing foci. This study shows that histologically incomplete lesions are effective means of blocking atrial conduction. Manasse and associates [13] also discussed the possibility that interruption of an electrical pathway as such may be effective without destruction of all fibers. Previous studies have indeed shown that gaps with an aperture of less than 5 mm in an atrial linear lesion block conduction [14]. This implies that electrophysiologic evaluation may be of great importance to show lesion efficacy. This study also suggests that the electrophysiologic measurements performed during ablation can predict the outcome of the lesions after several weeks, both histologically and electrophysiologically. However, further studies are needed to support this notion. The electrophysiologic measurements performed during ablation showed incomplete box lesions in 50% of the dogs after the first ablation, and only after repeated ablation was complete isolation achieved in 81% of the dogs. The success rate of 50% after the first ablation may indicate that the amount of microwave energy delivered may not have been sufficient to acquire optimal results. However, online electrophysiologic evaluation of the lesion can identify incomplete isolations with the possibility of repeating or lengthening the ablation interval and can dramatically increase the success rate. Electrophysiologic evaluation of lesions may also be of great importance to adapt the ablation procedure to the individual patient, because the thickness and composition of the human atrial wall strongly depend on age and disease progress. For example, thickening of the endocardium and atrial fibrosis has been shown in patients with mitral valve pathology. Failure to create transmural ablation lesions in the study of Santiago and associates [9] was also partly attributed to interindividual atrial differences caused by underlying cardiac pathology.

Clinical electrophysiologic measurements in the operating room need to be performed to study the efficacy of epicardial pulmonary vein isolation by different ablation devices in relation to human atrial pathology. We think that electrophysiologic measurements during pulmonary vein ablation as a control for lesion patency are easy to perform. Only a simple electrophysiologic recording and pacing system is needed inside the operating room. When good communication is present between the surgeon performing the ablation and the person performing the measurements, electrophysiologic lesion evaluation can be performed fast and effectively. In support of beating-heart off-pump procedures for AF, the combination of epicardial ablation and online electrophysiologic measurements may be the key for successful treatment.

A limitation of this study is that a relatively limited number of animals evaluated long-term were included. To study lesion evaluation in more detail, a study needs to be conducted that includes more animals that are killed at several time points. Also, this study did not compare the FLEX 10 microwave catheter with other epicardial ablation devices and energy sources. Because it is not unlikely that incompleteness of lesions may also be due to technical problems—such as poor catheter-tissue contact, poor overlap between lesions, or catheter twisting—other studies are needed to compare the efficacy of different ablation technologies and devices. Furthermore, the completeness of epicardial microwave ablation lesions assessed by histologic and electrophysiologic methods was studied in dogs. The dog atria, however, may not be comparable in size and thickness to the diseased atria of AF patients.

	Discussion

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
DR MICHAEL A. ACKER (Philadelphia, PA): It seems that you have answered the question of the first paper, perhaps, that the Columbia group, if they waited longer, 3 weeks, might have seen the histology of transmural damage in the dogs with block. It also speaks to the vital importance as we do more and more of these procedures to check for block in the operating room clinically. I know many groups do not do this. But it speaks to the potential importance of checking for block before we leave the operating room to improve our results.

DR MICHAEL ARGENZIANO (New York, NY): I really enjoyed that study. I appreciate your following up on our study only a few minutes later with the results that were requested.

I do want to clarify, based on your comments from a moment ago, that our chronic evaluation was actually at 4 weeks after the acute injury, so we did in fact wait for an appropriate amount of time as far as we could tell.

I do think that this is an interesting study, especially when juxtaposed with ours, because aside from showing in fact that transmurality, whether it is assessed acutely or chronically, may not be a perfect correlate to electrical isolation, the point that the authors make, I think, is an extremely important one, which is that we have to have a way in the operating room to assess the effectiveness of our lesions. Ultimately, whether or not acute histologic transmurality is achieved in the operating room really does not matter if we cannot assess it, and certainly I do not think that we are going to be in a position to take biopsy samples in the operating room. So I do think that it is quite fortunate that electrical isolation—which can be assessed, as the authors have shown and as we have done in the operating room—is the right way to go.

My question for the authors is, what happened to the 3 animals in which you were not able to achieve electrical isolation, even with up to 3 repeated ablations? Did those animals progress to histologic transmurality as well, and did any of the animals who were not electrically isolated in the acute setting progress to electrical isolation in the chronic setting?

Thank you.

DR VAN BRAKEL: Thank you for your question. Two of the 3 dogs with noncomplete electrophysiologic isolations were evaluated acutely and not chronically. Therefore, progress from noncomplete toward complete lesions could not be studied in these dogs. In the third dog with incomplete isolation, still-incomplete electrophysiologic isolation and a low percentage of transmural and circumferential tissue damage were observed 2 weeks after the procedure.

With regard to your comments on intraoperative measurements, I indeed do think that it can markedly optimize the surgical isolation of the pulmonary veins because the surgeon can adapt the ablation to the individual patient. We know that the atrial composition and wall thickness can differ between patients because of age and underlying cardiac disease. Therefore, intraoperative electrophysiologic measurements could provide the possibility of adapting the ablation time or the amount of energy to the individual patient, thus resulting in an electrophysiologically guided effective isolation of the pulmonary veins.

	Acknowledgments

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
The authors thank Cardio Tek for the kindly provided electrophysiologic measurement system (Eptracer38).

	References

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Gil Bolotin L. Wiley Nifong Jos G. Maessen Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by van Brakel, T. J. Articles by Maessen, J. G. Search for Related Content PubMed PubMed Citation Articles by van Brakel, T. J. Articles by Maessen, J. G. Related Collections Electrophysiology - arrhythmias