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Ann Thorac Surg 2007;83:538-541
© 2007 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Intraoperative Epicardial Electrophysiologic Mapping and Isolation of Autonomic Ganglionic Plexi

Department of Surgery, Section of Cardiothoracic Surgery, University of Cincinnati, Cincinnati, Ohio

Accepted for publication September 1, 2006.

^_* Address correspondence to Dr Mehall, Section of Cardiothoracic Surgery, University of Cincinnati, 231 Albert B. Sabin Way, PO Box 670558, Cincinnati, OH 45267 (Email: john.mehall{at}uc.edu).

Presented at the Poster Session of the Forty-second Annual Meeting of The Society of Thoracic Surgeons, Chicago, IL, Jan 30–Feb 1, 2006.

Drs Schneeberger and Wolf disclose that they have a financial relationship with Atricure, Inc.

 

	Abstract

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
BACKGROUND: Autonomic ganglionic plexi (GPs) have been implicated as triggers in lone atrial fibrillation (AF). The purpose of this study was to describe the technique and results of epicardial electrophysiologic mapping and the early effects of GP isolation.

METHODS: Intraoperative epicardial electrophysiologic mapping was performed on 41 consecutive patients during a stand-alone minimally invasive operation for AF. A map labeling anatomic locations was developed to describe the findings. Intraoperative high-frequency stimulation (800/minute, 12 to 16 mA, pulse duration 9.9 ms) was performed using a standard quadripolar catheter placed directly on the epicardium. Locations where stimulation resulted in ventricular slowing with doubling of the electrocardiographic R-R interval were defined as active GPs. These areas were mapped and described. After dry bipolar radiofrequency isolation, the sites were again stimulated to assess isolation.

RESULTS: Forty-one patients (mean age of 60.2 years, 31 males) underwent operation for AF (28 intermittent AF, 13 chronic). Active GPs were identified in all patients (24 bilateral, 17 unilateral). There was a mean of 5.0 GPs on the right and 2.7 on the left. More than 50% of patients had active GPs along the interatrial groove on the right and along the ligament of Marshall. All sites were inactive after radiofrequency isolation. Six-month follow-up is available for 15 patients, with 14 patients free of AF.

CONCLUSIONS: Autonomic GPs can be routinely identified during AF surgery utilizing high-frequency stimulation. The GPs are clustered around the interatrial groove and the ligament of Marshall, and the cardiac response to GP stimulation can be eliminated with bipolar radiofrequency isolation. The addition of GP isolation to bilateral pulmonary vein isolation may increase freedom from AF.

Extensive research has been done in recent years to elucidate the cause or causes of atrial fibrillation owing to the large health burden this condition imposes. Much of this research has focused on ectopic electrical foci based on the landmark paper of Haissaguerre and colleagues [1] describing ectopic triggers in the pulmonary veins. Even before the development of interest in pulmonary vein triggers, however, epicardial innervation was already known to have effects on cardiac rate and rhythm. The control of cardiac function by the nervous system is regulated through epicardial ganglionic plexi (GP), which contain efferent parasympathetic, efferent sympathetic, and afferent neurons [2] and are found primarily in fatty epicardial tissues on the upper half of the heart [3]. Ganglionic plexi become activated in response to changing cardiovascular physiology, and this activity results in changes in cardiac rate and rhythm, including the induction of atrial fibrillation [4, 5].

Given these effects of GP, and the observations of Scherlag and associates [6] based on work with canines, we undertook a study to map epicardial GP and to describe their location as well as effects of electrical isolation of the plexi in patients undergoing operation for the treatment of lone atrial fibrillation.

	Material and Methods

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The Institutional Review Board of the University of Cincinnati approved the study protocol, the operative procedure, and the consent form and process. Patients were informed of all options for treatment of atrial fibrillation (medical, catheter based, and all surgical options) and that ganglioninc plexi mapping and isolation or ablation were currently being studied. Patients were also informed that there was no current definitive evidence supporting the role of the GP in atrial fibrillation causation or treatment, but that animal and preliminary human research data were suggestive of a role.

The study was conducted on consecutive patients who were undergoing surgical treatment of lone atrial fibrillation through a bilateral thoracoscopic assisted approach [6]. All patients had failure, intolerance, or refusal of medical antiarrhythmic therapy or complications of anticoagulation, or both. Patients underwent intraoperative epicardial electrophysiologic mapping at the time of operation to determine the location and activity of GP. Based on the location of GP in canines [3], a schematic diagram of the bilateral pulmonary vein orificies was developed by Ben Scherlag, Warren Jackman, and colleagues (personal communication, November 2004) to more accurately describe the area being mapped (Fig 1). All stimulation and mapping were performed before any dissection or ablation. The complete procedure was performed on the right side first, followed by the left side. Intraoperative epicardial electrophysiologic mapping was performed using a standard 5F electrophysiology catheter (St. Jude Medical, Minneapolis, Minnesota). The distal electrode was used to deliver high-frequency stimulation at a rate 800/minute, amplitude of 12 to 16 mA, with a pulse duration of 9.9 ms (Medtronic, Minneapolis, Minnesota) to specific areas as depicted in the epicardial diagram. The electrocardiogram was monitored, and stimulation that resulted in a doubling of the electrocardiographic R-R interval was deemed to represent a location of active GP.

View larger version (21K): [in this window] [in a new window]   Fig 1. Diagram of epicardial mapping locations. (IVC = inferior vena cava; L = left; LA = left atrium; LIPV = left inferior pulmonary vein; LSPV = left superior pulmonary vein; LV = left ventricle; R = right; RA = right atrium; RIPV = right inferior pulmonary vein; RSPV = right superior pulmonary vein; SVC = superior vena cava.)

After pulmonary vein isolation, GP that had preablation activity were restimulated to confirm their ablation or isolation. If GP remained active, the radiofrequency lesions were repeated or the epicardial tissue was directly ablated with bipolar electrocautery. Areas of active GP that were on the atrioventricular node side of the area of isolation were ablated using bipolar electrocautery directly on the epicardium.

	Results

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
During the study period, 41 patients underwent intraoperative epicardial electrophysiologic mapping. There were no deaths or complications in this group of patients. Specifically, epicardial mapping and ablation of GP resulted in no problems in any patient other than transient lengthening of the R-R interval during stimulation, which was well tolerated routinely. The additional time required to perform epicardial mapping, ablation of GP, and repeat stimulation and confirmation of bidirectional electrical isolation was, on average, approximately 20 minutes. No patient required a pacemaker after the procedure.

The average age was 60.2 years, and 31 were male. Paroxysmal atrial fibrillation was present in 28 patients, and 13 had chronic atrial fibrillation on 10–14 days of preoperative continuous home monitoring. A mean of 3.0 active GP were identified in each patient, with a mean of 5.0 active GPs on the right (range, 0 to 10) and 2.7 active GPs on the left (range, 0 to 8). Active GP were found bilaterally in 24 patients and unilaterally in 17 patients, 14 with only right-sided activity and 3 with only left-sided activity. The incidence of activity by epicardial location is shown in Table 1. The greatest concentration of active GP was in the areas of the superior aspect of the interatrial groove and the ligament of Marshall. Radiofrequency ablation was performed one to four times at each site to achieve complete isolation. After radiofrequency isolation, all sites outside the area of isolation were unable to elicit ventricular rate changes in response to high-frequency stimulation.

	Comment

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Recent evidence has suggested a synergistic relationship between GP activity and ectopic pulmonary vein foci to lower the threshold of inducibility for atrial fibrillation [6, 7]. Stimulation of ectopic pulmonary vein triggers, when combined with stimulation of adjacent GP, induces atrial fibrillation at lower thresholds and at lower amplitude than when pulmonary veins are stimulated alone. In addition, when GP and pulmonary veins are stimulated in combination, atrial fibrillation can be induced by pulmonary vein foci that cannot induce atrial fibrillation when stimulated alone [8]. Thus, activation of GP results in a progressive and significant decrease in atrial refractoriness that lowers the threshold for induction of atrial fibrillation [7]. In addition, the neural input of GP remains active even after extracardiac denervation [9].

Several clinical studies have also provided indirect evidence for the synergy between pulmonary vein triggers and GP [6, 10]. Destruction of GP alone rendered 96% of patients noninducible to atrial fibrillation [11]. Some patients undergoing catheter-based radiofrequency ablation were noted to have a "vagal" response with ventricular slowing during the ablation that resolved as the isolation was completed [10]. The authors assumed that this was due to stimulation of GP during the start of isolation, followed by eventual destruction of the plexi and loss of GP activation. In follow-up, patients who had exhibited the "vagal" response had a significantly higher freedom from atrial fibrillation [10]. This finding has also been reported by others [6].

When performed alone, surgical pulmonary vein isolation typically yields cure rates of less than 90% [12]. These results, combined with the growing knowledge of the synergy between GP and pulmonary vein inducibility, have led our group to add routine epicardial mapping and isolation/ablation of GP to our surgical treatment of atrial fibrillation. The results of this study suggest that epicardial mapping of GP can be performed safely and easily, and that all patients have at least some active GP. Active GP are usually located in epicardial fat pads along the interatrial groove in the right side of the heart, and along the ligament of Marshall on the left. Often, the location of these active GP is outside the areas traditionally isolated when pulmonary vein isolation alone is performed. The persistent activity of these unisolated active GP may help to explain the 10% to 40% recurrence rate of atrial fibrillation after pulmonary vein isolation alone [12]. When active GP are within tissue that is isolated using dry bipolar radiofrequency ablation, their effects on cardiac rate and rhythm are extinguished. In addition, it is important to note that epicardial GP can also be destroyed by the epicardial application of bipolar electrocautery.

Thus far in our experience, the use of bipolar radiofrequency pulmonary vein isolation, mapping and ablation of GP, and excision of the left atrial appendage has proven to be safe and efficacious. No patients have died or have had complications, and preliminary follow-up data suggest that the procedure has resulted in a greatly reduced burden of atrial fibrillation in our patients. No patient has experienced a documented episode of reentrant arrhythmia, and no patient has exhibited evidence of reduced chronotropic responsiveness. Thus far we have seen no functional damage to the left atrium during follow-up. We believe that subsequent follow-up and the accumulation of additional data will document long-term results that are comparable to or perhaps even superior to those achieved by the utilization of alternative techniques. In our opinion, the addition of autonomic ablation will likely lead to improved long-term results and may reduce the propensity for the development of atrial flutter. The long-term results regarding the development of pulmonary vein stenosis are unknown; however, we do not anticipate any increased risk as a result of our technique. Previous short-term follow-up demonstrated no evidence of pulmonary vein stenosis in similar patients undergoing bilateral pulmonary vein isolation [7].

As the surgical treatment of atrial fibrillation continues to evolve, the detection and ablation of active GP should be further studied. Once sufficient numbers of patients have been treated using techniques that address the GP, the significance of their effects and the potential for increased freedom from atrial fibrillation can be better assessed. Currently, the long-term effects of extinguishing active GP on the recurrence rate of atrial fibrillation postoperatively are not known. Although we believe that GP ablation will increase the freedom from atrial fibrillation, follow-up length and patient volume are still insufficient for definitive conclusions. When we have accumulated additional data, we hope to make them the basis of a subsequent report.

	Acknowledgments

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
The authors would like to thank Pamela Daniel, RN, for her assistance in conducting this study.

	References

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

1. Haissaguerre M, Jais P, Shah DC, et al. Spontaneous initiation of atrial fibrillation by ectopic beats originating in the pulmonary veins N Engl J Med 1998;339:659-667.[Medline]
2. Armour JA, Hopkins DA. Activity of canine in situ left atrial ganglion neurons Am J Physiol 1990;259:1207-1215.
3. Yuan BX, Ardell JL, Hopkins DA, Losier AM, Armour JA. Gross and microscopic anatomy of the canine intrinsic cardiac nervous system Anat Rec 1994;239:75-87.[Medline]
4. Ali IM, Butler CK, Armour JA, Murphy DA. Modification of supraventricular arrhythmias by stimulating atrial neurons Ann Thorac Surg 1990;50:251-256.[Abstract/Free Full Text]
5. Coumel P. Paroxysmal atrial fibrillation: a disorder of autonomic tone Eur Heart J 1994;15(Suppl A):9-16.[Abstract]
6. Scherlag BJ, Nakagawa H, Jackman WM, et al. Electrical stimulation to identify neural elements on the heart: their role in atrial fibrillation J Intervent Card Electrophysiol 2005;13:1-6.
7. Wolf RK, Schneeberger EW, Osterday R, et al. Video-assisted bilateral pulmonary vein isolation and left atrial appendage exclusion for atrial fibrillation J Thorac Cardiovasc Surg 2005;130:797-802.[Abstract/Free Full Text]
8. Nakagawa H, Scherlag BJ, Aoyama H, et al. Catheter ablation of cardiac autonomic nerves for prevention of atrial fibrillation in a canine model Heart Rhythm 2004;1(Suppl):S10.
9. Ardell JL, Butler CK, Smith FM, Hopkins DA, Armour JA. Activity on in vivo atrial and ventricular neurons in chronically decentralized hearts Am J Physiol 1991;260:713-721.
10. Pappone C, Santinelli V, Manguso F, et al. Pulmonary vein denervation enhances long-term benefit after circumferential ablation for paroxysmal atrial fibrillation Circulation 2004;109:327-334.[Abstract/Free Full Text]
11. Platt M, Mandapati R, Scherlag BJ, et al. Limiting the number and extent of radiofrequency applications to terminate atrial fibrillation and subsequently prevent its inducibility Heart Rhythm 2004;1(Suppl):S10.
12. Misaki T, Fukahara K. Recent topics on the surgical treatment for atrial fibrillation Ann Thorac Cadiovasc 2004;10:277-280.

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