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Ann Thorac Surg 2005;80:881-887
© 2005 The Society of Thoracic Surgeons

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Original article: Cardiovascular

Post-Mortem Histologic Evaluation of Microwave Lesions After Epicardial Pulmonary Vein Isolation for Atrial Fibrillation

^a Department of Cardiothoracic Surgery, University Hospital Maastricht, Cardiovascular Research Institute Maastricht, Maastricht, the Netherlands
^b Department of Pathology, University Hospital Maastricht, Cardiovascular Research Institute Maastricht, Maastricht, the Netherlands

Accepted for publication March 16, 2005.

^_* Address reprint requests to Dr Maessen, Department of Cardiothoracic Surgery, University Hospital Maastricht, P. Debyelaan 25, Postbus 5800, 6202 AZ Maastricht, the Netherlands; (Email: j.maessen{at}scpc.azm.nl).

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
BACKGROUND: Surgical pulmonary vein isolation has gained widespread use as a treatment modality for patients with concomitant atrial fibrillation. However, several uncertainties persist concerning the appropriate energy source, approach, and the need for lesion transmurality. In this study, we present an in-depth histologic investigation of epicardial ablation lesions in 3 patients.

METHODS: Within a large clinical series of adjuvant epicardial beating-heart microwave isolation of the pulmonary veins, with intraoperative measurement of electrical block, 3 nonablation-related deaths allowed detailed histologic investigation of the lesions. All three patients were in sinus rhythm prior to death. Transmural histologic sections from the box lesion encircling the pulmonary veins were microscopically examined for tissue damage, lesion depth, width, and transmurality, as well as for signs of ongoing repair.

RESULTS: Three out of 13 tissue samples showed transmural lesions. In three sections no histologic damage was observed and in the remaining samples transmural extent of myocardial damage ranged from 48% to 82% (mean, 64 ± 13%). Lesion depths varied between 1.2 mm and 5.7 mm (mean 2.6 ± 1.3 mm). The lesion depth did not differ significantly among patients and was not related to the thickness of the epicardial or myocardial layers. Interestingly, several sections showed clear necrosis of nerve bundles located in the epicardial tissue.

CONCLUSIONS: This post-mortem histologic study showed that in the majority of samples the lesions were not transmural and that the extent of myocardial damage was highly variable. Even in this validated approach of epicardial beating heart ablation with satisfactory clinical results, transmurality of lesions cannot be assumed.

	Introduction

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Surgical pulmonary vein isolation has gained widespread use as a treatment modality for patients with concomitant atrial fibrillation (AF) undergoing cardiac surgery. Part of the increased interest for this therapy is the availability of new energy-based ablation tools, which allow the development of minimally invasive strategies, including beating-heart epicardial ablation. Different energy sources such as microwave, cryothermia, radiofrequency, laser, and ultrasound have been used in clinical and preclinical settings [1]. The aim of all these ablation tools is to achieve transmural lesions in a safe and reproducible manner. However, several uncertainties persist concerning the appropriate energy source, approach (epicardial versus endocardial) and the need for transmurality [2, 3]. Previous studies extensively evaluated ablation lesions using electrophysiologic and histologic methods. However, only histologic evaluation of acute lesions has been performed in patients, taking biopsies at limited places [4, 5]. Since experimental studies suggest that lesions evolve during the first days to a month after the ablation, histologic characterization of the evolving lesion may be more representative than acute evaluation [6].

The purpose of this study was to evaluate transmurality of evolving lesions after beating-heart pulmonary vein isolation using microwave energy in patients. During the extensive experience obtained at our center using microwave energy for adjuvant beating-heart pulmonary vein isolation, some nonablation-related deaths occurred. Post-mortem investigation of the lesions was performed in three cases. Our findings are discussed in light of the current debate concerning the actual working mechanism of AF abolishment by pulmonary vein isolation.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
In a series of 140 patients who underwent adjuvant pulmonary vein isolation, 12 nonablation-related deaths occurred, of which autopsy permission was obtained in 3 cases (Table 1 ). The first patient (A), an 80 year old male with a history of paroxysmal AF, underwent coronary artery bypass grafting, aortic valve replacement, and pulmonary vein isolation. After an uncomplicated first nine days postoperatively, the patient was resuscitated after sudden cardiac arrest. This was due to hypoxia caused by aspiration and sputum retention. The patient suffered from a postanoxic encephalopathy and died on the 17th day postoperatively due to progressive respiratory insufficiency. This patient showed several short episodes of postoperative AF but was in sinus rhythm prior to death.

The third patient (C) was a 63 year old male with coronary artery disease and permanent AF. After coronary artery bypass grafting and pulmonary vein isolation this patient remained hemodynamically unstable due to persistent bleeding, with progression of preexisting renal dysfunction. After full recovery, the patient died suddenly of unknown cause on the 22nd day after surgery. Also in this patient, sinus rhythm was restored successfully.

Ablation Procedure
Off-pump beating-heart ablation around the pulmonary veins was performed by a single experienced surgeon (JGM), prior to concomitant operation. After standard sternotomy and opening of the pericardial sac, the pericardial reflection between the superior caval vein and the superior right pulmonary vein was dissected, giving access to the transverse sinus. The oblique sinus was entered by dissecting the reflection between the inferior caval vein and the inferior right pulmonary vein. Epicardial ablation was performed using either the Flex 4 (patients A and C) or the Flex 10 microwave energy catheter (Guidant, Afix, Fremont, CA). The Flex 4 catheter is a surgical ablation probe on a malleable shaft, which enables single energy applications of 60 millimeters, while the Flex 10 catheter is a flexible catheter, which can be positioned around the pulmonary veins in a lasso-like fashion ensuring continuity of up to ten lesions. Both tools were used to construct a box lesion, encircling all four pulmonary veins, by a series of single energy applications of 65 Watts for 90 seconds (Fig 1). Adequate energy delivery was confirmed by observing an increase of tissue surface temperature after every energy application. Intraoperative measurements were performed using temporary epicardial pacing wires and a data acquisition system for electrogram recording and bipolar pacing (Eptracer38, Cardiotec, Beek, The Netherlands). Exit blocks were confirmed by loss of capture outside the box lesion when pacing from inside the box lesion (output set at 4 times the pacing threshold). A more in-depth description of the procedure was provided in a previous report [7].

View larger version (61K): [in this window] [in a new window]   Fig. 1. Posterior view of the heart. The dotted line illustrates the ablation line encircling all four pulmonary veins (left pulmonary veins = LPVs; right pulmonary veins = RPVs). Arrows mark pericardial reflections between the pulmonary veins and the caval veins that are opened in order to enter the transverse and oblique sinus. Roman figures I to V mark the sampling site at, respectively, the cranial, medial, caudal, laterocaudal, and lateral part of the ablation lesion. (SCV = superior caval vein; ICV = inferior caval vein.)

Statistics
Tissue thickness, lesion depth, and lesion width are expressed in millimeters and the means ± standard deviations are provided. Metric variables from the three patients were compared using a Wilcoxon rank sum test and were considered statistically significant if the p value was less than 0.05. Correlation between metric variables and transmurality was examined, using the Spearman’s rank correlation test for nonparametric variables, in SPSS 10.1 statistical software (SPSS, Chicago, IL).

	Results

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
The ablation lesion could be identified macroscopically as a blanched continuous line with ill-defined borders. Clear fibrin deposition over the whole surface of the epicardium was noted, especially in those cases of late mortality (patients A and C).

Microscopic Findings
Ablation damage was characterized in the epicardial layer by adipose tissue necrosis and intercellular edema. Within the myocardial layer signs of microwave ablation damage were found depicting myocyte necrosis defined as coagulation necrosis (Fig 2). Toward the border of the endocardium several samples from patients A and C, who, respectively, died on the 17th and 22nd day after the operation, showed focal areas of granulation tissue. These areas were mainly located at the borders of the damaged myocardial tissue, especially towards the endocardium. The endocardium itself showed no ablative damage; ie, no disruption of the inner surface. Interestingly, several sections showed clear signs of coagulation necrosis of nerve bundles and small vessels located in the epicardial tissue (Fig 3).

View larger version (159K): [in this window] [in a new window]   Fig. 2. Necrotic myocytes (arrows) showing loss of nuclei, and homogeneous and hypereosinophilic cytoplasm. The left part of this illustration shows epicardial fat tissue. (Hematoxylin and eosin staining; bar = 100 µm).

View larger version (158K): [in this window] [in a new window]   Fig. 3. Necrotic nerves bundles (arrows) in epicardial layer at the border with nonviable myocardium. (Hematoxylin and eosin staining; bar = 100 µm).

Lesion Depth, Width, and Transmural Extent of Lesions
Three of the 13 samples (23%) showed transmural lesions extending from the epicardium and full thickness of the myocardium, but without affecting the endothelial surface (Fig 4). In the other 7 samples with ablative damage the transmural extent of myocardial damage ranged from 48% to 82% (Fig 5). Three sections (23%) showed no histologic damage; namely, two samples collected from the left atrial roof from patients A and patient B, and one sample excised from the lateral border of the lesion set in patient B, between the orifice of the left inferior pulmonary vein and the atrioventricular groove. Although sampling was repeated to rule out a sampling error, it remained impossible to identify clear signs of ablative damage from these sites and in these patients. Table 2 gives an overview of the measured diameters of atrial wall layers, as well as lesion depth, width, and transmural extent of myocardial damage, in all the collected samples.

View larger version (171K): [in this window] [in a new window]   Fig. 4. Transmural lesion reaching through the whole myocardial layer to the endocardial border without disruption of the endocardial surface (Endo). (Hematoxylin and eosin staining;, bar = 100 µm).

View larger version (154K): [in this window] [in a new window]   Fig. 5. Overview of nontransmural lesion showing a strip of vital myocardium persisting at the border with the endocardial layer. The arrow marks the extension of the ablation lesion. (Endocard = endocardium; Epicard = epicardium; Myocard = myocardium.) (Hematoxylin and eosin staining; bar = 400 µm).

	Comment

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Reported success rates of surgical pulmonary vein isolation in patients with underlying structural heart disease range from approximately 68% to 92% sinus rhythm restoration [8–12]. The development of epicardial approaches has allowed beating-heart ablation, without compromising clinical outcome or safety. A previous study from this institution showed that using microwave ablation, electrical isolation of the pulmonary veins could be achieved epicardially without cardiopulmonary bypass support [7]. Sixty-seven percent to 76.2% of the patients were in normal sinus rhythm at a follow-up of 15.2 months, depending on the underlying pathology [13]. The principle finding of this post-mortem evaluation of lesions, sampled at different sites of ablation lines, is that only 23% of these samples were transmural. In another 23% of samples no ablative damage could be identified, and in the remaining samples transmural extent of myocardial damage ranged from 48% to 82%.

Several other studies have shown that achieving transmurality in a reliably and reproducible manner remains difficult, especially using epicardial beating-heart approaches [4, 5, 14, 15]. Thomas and colleagues [14] used a sheep model to compare radiofrequency epicardial ablation on the beating heart, with endocardial ablation after cardioplegia. They found that only 13% of all epicardial lesions were transmural compared with 92% of the endocardial lesions. Santiago and colleagues [5] found that only 3 out of 38 lesions examined were transmural after epicardial radiofrequency ablation on the beating heart in patients with underlying valve pathology. All publications discussing epicardial lesions involve animal studies, or studies on human tissue sampled immediately after ablation. Therefore, the studies did not address time-related processes involving inflammation and lesion evolvement. This study is a post-mortem evaluation of evolving ablation lesions performed in a normal clinical setting, using a clinically validated approach of epicardial beating-heart microwave ablation for AF.

Determinants of Extent of Ablative Damage
In each patient an example of complete transmural tissue damage was found, demonstrating that it is possible to achieve transmurality. In order to identify factors that determined the ability to achieve transmural lesions, we investigated how lesion depth correlated with epicardial, myocardial, and endocardial layer thickness. As might be expected, thicker epicardial and myocardial layers resulted in less deep ablation lesions.

Interestingly, we observed that all the lesions were more wide than deep. The ideal lesion should penetrate deep enough to cause transmurality, but be as narrow as possible to limit redundant damage to viable myocardial tissue [14]. We hypothesized that the broad lesions could be a direct result of the ablation being performed on the beating heart, with consequently poor fixation of the catheter. However, even though this might be the case, the lesion width did not correlate to the lesion depth, and therefore this does not explain the difficulties with achieving transmurality. In fact, Thomas and colleagues [14] also observed that all lesions were wider then they were deep. The lesions they applied on the endocardium after cardioplegia were, however, wider then the epicardial lesion. They believed that the most important factor limiting lesion depth and consequently transmurality in epicardial beating-heart ablation is the presence of epicardial fat and endocardial cooling by circulating blood.

In three sections no ablative damage could be detected. This finding might be explained by discontinuity of the ablation line, since repeated sampling made a sampling error unlikely. One of the three samples was sampled between the orifice of the left inferior pulmonary vein and the atrioventricular groove, also known as the left atrial isthmus, which is considered a difficult site to ablate. At this site there is no visual confirmation of overlapping placement of the catheter. Even if the Flex 10 catheter is used, which ensures continuity of the lesion, twisting of the catheter and loss of tissue contact can always occur and will be difficult to detect.

Discrepancy Between Initial Electrophysiologic Endpoint of Treatment and Post-Mortem Histologic Findings
Although our method of pulmonary vein isolation included intraoperative measurement of exit block, post-mortem histologic finding showed nontransmural lesion in a majority of cases. This discrepancy between electrophysiologic and histologic findings was also reported by van Brakel and colleagues [15]. During robot-assisted pulmonary vein isolation in dogs, 12 out of 16 procedures resulted in a bidirectional block of conduction. However, of these electrophysiologically complete ablations, the mean transmurality was only 33%. In dogs that were evaluated chronically, the lesion remained electrophysiologically complete, while transmurality increased substantially to 66%.

Explanations for the observed difference between histologic and electrophysiologic findings might include the following. (1) The persistence of gaps with an aperture of less then 5 mm, which are known to be able to interrupt electrical pathways. This mechanism has been described in discontinuous lesions in dogs [16]. Nontransmural lesions, thus the persistence of a layer of viable myocardial fibers, might have the same electrophysiologic effects as discontinuous lesions. (2) The functional impairment of myocytes not accompanied by morphologic changes. (3) Elevation of the pacing threshold within the box lesion, which creates the impression of an exit block. (4) Insufficient sensitivity of used method to detect myocardial damage. An important difference with the previous finding of van Brakel and colleagues [15] is that this histologic evaluation was performed 2 to 22 days after the intraoperative measurement of conduction blocks. Therefore, reconduction over the ablation lesion at the moment of death must also be considered.

Evolution of Epicardial Lesions
Since two patients died more then two weeks after operation we were able to examine late reactive changes after the inflicted ablation damage. Indeed, samples from these two patients depicted more signs of inflammation and ongoing repair. These focal areas were found within damaged myocardium, but primarily at borders with viable myocardium or endocardium, since the process of granulation is mediated from viable sites.

Several interesting questions remain concerning the early recovery of damaged myocytes and their role in possible reconduction over the ablation line. Even though strips of myocardium within the nontransmural lesions showed no apparent signs of damage, some of these myocytes might have survived acute ablation damage. Manasse and colleagues [17] observed "viable looking" cells within heavily severed tissue directly after microwave ablation and proposed a possible role for these cells in delivering electrical reentry activity associated with AF.

Substrate Modification Might Contribute to Clinical Success of Surgical Pulmonary Vein Isolation
The rationale of pulmonary vein isolation as a cornerstone of invasive strategies for AF treatment was provided by Haissaguerre and colleagues [18]. They not only identified triggers within the pulmonary veins initiating paroxysms of atrial fibrillation, but were also able to demonstrate how extinguishing these triggers abolished AF. Producing transmural lesions was therefore considered crucial to preventing pulmonary vein triggers from initiating AF. Even though several studies showed that transmurality can be difficult to obtain, the true discrepancy with the satisfactory clinical results was highlighted only recently by Stabile and colleagues [3]. Performing circumferential radiofrequency ablation of pulmonary vein ostia with an anatomic approach, they found that although 80% of the patients were free of atrial arrhythmias, only 40% of the mapped pulmonary veins were electrically isolated. Kottkamp and colleagues [19] also demonstrated that even though less then 20% of their circular lesions resulted in complete pulmonary vein isolation, the freedom from AF after 12 months measured 74% according to 7 days electrocardiographic monitoring.

The observation of frequently incomplete lesions on the one hand, and numerous reports of satisfactory results on the other, raises the question whether transmural lesions are necessary and whether trigger isolation is the sole mechanism of AF abolishment after pulmonary vein isolation. Several alternative working mechanisms have been proposed and were summarized by Stabile and colleagues [3]; namely, the modification of substrate of pulmonary vein tachycardia or mother waves making reentry pathways unsuitable, denervating effects, damage to Marshall’s ligament and Bachmann’s bundle, and promotion of atrial electroanatomic remodeling. A previous study of this institute provided data demonstrating the important role of substrate modification. In this dog model for acute AF, it was shown that, even after an intentionally incomplete lesion encircling the pulmonary veins, AF duration decreased and the AF-cycle length increased [20] .

We would like to emphasize that, especially, the denervating effect involving epicardial fat pads containing parasympathic nerves and damage to specialized conduction structures involved in AF might be of crucial importance in epicardial ablation. In fact, in this study multiple sections with necrotic nerve branches within the epicardium were found.

Study Limitations
A clear limitation of this post-mortem study is the limited number of cases. However, these three cases gave us this unique opportunity to evaluate microwave lesions applied under normal clinical conditions. Second, the rhythm outcome of these specific patients has to be interpreted with care, since all three patients died relatively early after the procedure.

Moreover, two out of three patients were still on antiarrhythmic medication at the moment of death. Therefore, this study does not provide the answer to the question whether complete isolation of pulmonary veins is essential for curing AF.

In conclusion, even in this validated approach of epicardial beating-heart ablation with good clinical results, transmural myocardial damage cannot be assumed. The working mechanism of epicardial pulmonary vein isolation might involve not only isolation of triggers, but also modification of the AF substrate. More insight into the effect of epicardial pulmonary vein ablation on the pathophysiologic mechanisms involved in AF is necessary to understand and to optimize the clinical results.

	Acknowledgments

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
We would like to thank Dr Randolph Statius van Eps for thoroughly reading the manuscript and providing critical comments and suggestions.

	References

Top Abstract Introduction Patients and Methods Results Comment 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): Ryan E. Accord Jos G. Maessen Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Accord, R. E. Articles by Maessen, J. G. Search for Related Content PubMed PubMed Citation Articles by Accord, R. E. Articles by Maessen, J. G. Related Collections Electrophysiology - arrhythmias