A atrial rate of 250 to 350 beats per minute that usually

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1 Use of Intraoperative Mapping to Optimize Surgical Ablation of Atrial Flutter Shigeo Yamauchi, MD, Richard B. Schuessler, PhD, Tomohide Kawamoto, MD, Todd A. Shuman, MD, John P. Boineau, MD, and James L. Cox, MD Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri The purpose of this study was to develop a surgical treatment for atrial flutter using intraoperative activation sequence mapping to minimize the surgical procedure necessary to ablate the flutter. A canine model (n = 10) of left atrial enlargement was developed by creating a shunt from the left subclavian artery to the left superior pulmonary vein. Sustained atrial flutter was easily induced in this model. The flutter consisted of a single reentrant circuit that rotated around one or two anatomic obstacles linked by a region of functional block. Epicardial templates, consisting of 252 bipolar electrodes, were used to record activation time maps. After localization of the reentrant circuit, surgical incisions were placed to inter- rupt the pathways. In all 10 animals, flutter could be induced and intraoperative mapping localized the reentrant circuit. Seven circuits were in the right atrium and three were in the left atrium. The operation ablated all of the preoperative circuits. However, in 5 of the animals, flutter originating from a new circuit could be induced. Activation sequence mapping before and after operation demonstrates that there are multiple potential reentrant pathways in this canine model of atrial flutter. Therefore, all potential pathways must be surgically interrupted to prevent inducibility of atrial flutter. ( 1993;56:33742) trial flutter is a regular atrial tachycardia with an A atrial rate of 250 to 350 beats per minute that usually conducts to the ventricles in a 2:l ratio. Electrophysiologic studies in both humans and animal models have demonstrated that flutter is a reentrant arrhythmia that is characterized by one stable macroreentrant loop [l-81. Mapping studies in humans have suggested that the reentrant loop encircles the inferior and superior vena cava, rotating in a clockwise or counterclockwise direction (1-31. Animal studies have suggested that reentrant loops can also include the pulmonary veins on the left atrium, as well as reentrant loops that rotate around a region of functional block in the posterior right atrium [4-81. Because flutter is generated by a single stable macroreentrant loop, it was anticipated that it would be amenable to surgical ablation. However, only a limited number of attempts at surgical ablation have been reported [l, 91. The purpose of this study was to develop a surgically ablative procedure for atrial flutter that minimized the amount of operation necessary by use of intraoperative mapping. To accomplish this, a shunt was created in dogs between the subclavian artery and the left superior pulmonary vein to produce chronic left atrial pressure and volume overload. This model of left atrial enlargement and hypertrophy created the substrate for atrial flutter. Accepted for publication Dec 3, Address reprint requests to Dr Cox, Division of Cardiothoracic Surgery, Washington University School of Medicine, Suite 3108, Queeny Tower, Box 8109, St. Louis, MO Material and Methods Ten adult mongrel dogs weighing between 25 and 35 kg were anesthetized with thiopental sodium (20 to 30 mgkg intravenously) and maintained with 1% to 2% halothane. Positive-pressure ventilation was maintained via a cuffed endotracheal tube at an inspired oxygen concentration of 50%. A 6F Swan-Ganz catheter was inserted through the right femoral vein, and an 18-gauge needle was placed into the femoral artery to monitor systemic blood pressure. The lead I1 electrocardiogram was continuously monitored. The chest was opened through a left thoracotomy via the fourth intercostal space. Through a pursestring suture in the left middle pulmonary artery and vein, Millar transducer catheters were passed into the left atrium, left ventricle, and pulmonary artery for continuous monitoring of these pressures. The subclavian artery was prepared for the shunt procedure. After intravenous heparin (0.05 mg/kg) was administered, the internal thoracic vertebral, costocervical, and omocervical arteries were ligated and divided to obtain a suitable length of subclavian artery to perform the shunt. The left subclavian artery was anastomosed to the left superior pulmonary vein from end to side at the point where it crosses to enter the pericardium. After measurement of the hemodynamic and electrophysiologic data, the thoracotomy was closed. Volume and pressure overload of the left atrium developed, and during a 3- to 5-month period, left atrium enlargement and hypertrophy developed. There was also and hypertrophy Of the right atrium. After this, the animals were easily inducible into sustained by The Society of Thoracic Surgeons /93/$6.00

2 338 YAMAUCHI ET AL OPETION FOR ATRIAL FLUTTER 1993; B Fig 1. The epicardial electrodes are shown on fixed canine atria. Panel A shows an anterior (ANT) view. A single template extends across the anterior atria from the right atrial appendage (A) to the left atrial appendage (A). Panel B shows a posterior view (POST). Two templates are used to cover the posterior surface On the posterior left atrium, a template extends from the A under the pulmonary veins (PV) to the inferior vena cava (IVC). The second posterior template covers the posterior right atrial surface. The black dots on each template represent the electrode position. (MV = mitral valve; SVC = superior vena cava; TV = tricuspid valve.) atrial flutter. Detailed electrophysiology of the induced flutter has been previously reported [8]. After the period of 3 to 5 months, the animals were reanesthetized with intravenous thiopental sodium (20 to 30 mg/kg) and maintained with 1% to ;!% halothane. Positive-pressure ventilation was administered via a cuffed endotracheal tube at an inspired oxygen concentration of 50%. The chest was opened through a right thoracotomy via the fifth intercostal space. Molded epicardial electrode templates with 252 electrode pairs were sutured to the right and left atria (Fig 1). Epicardial pacing electrodes were positioned on the right and left atrial appendages and the right ventricle. A standard lead I1 electrocardiogram and systemic arterial blood pressure were continuously monitored. Flutter was induced using programmed premature atrial stimulation at a basic cycle length of 300 milliseconds with a single or double premature stimulus deliv- ered at progressively shorter coupling intervals (10 milliseconds). If premature stimulation was unsuccessful, a 20-second burst of rapid pacing was begun at a cycle length of 200 milliseconds and progressively decreased in 10-millisecond decrements until sustained flutter occurred. Sustained flutter was defined as any run lasting longer than 5 minutes. Electrograms were recorded from all 252 points simultaneously during sinus rhythm, right and left atrial pacing, and induced flutter. A 256-channel computerized data acquisition and analysis system was used to collect, process, and display data. Bipolar electrograms were recorded at a gain of 1,000 with a frequency response of 10 to 500 Hz. Each channel was digitized at 1,000 Hz with a 12-bit resolution. Local epicardial activation times were determined from the maximum amplitude of the bipolar electrogram. All electrograms were edited visually to verify accuracy of the computer-picked activation times. These activation times were displayed on a schematic diagram of the atrium as activation time maps. Based on the activation sequence maps, a set of incisions was designed to ablate the flutter. In the first 2 dogs, minimum incisions were used to interrupt the reentrant circuit. However, the reentry and flutter subsequently recurred. In animals 3 through 8, more extensive incisions were made based on whether the flutter circuit was in the right or left atrium. If the flutter was in the right atrium, one set of incisions was used; if it was in the left, another set of incisions was used. Again, because of the high recurrence rate of flutter, in dogs 9 and 10, the combined right and left atrial incisions were used. Examples of those incisions are illustrated in Figures 2 through 5 and are discussed in further detail in the Results section. Intravenous heparin (1 mg/kg) was administered in the right femoral artery. Both venae cavae were cannulated for cardiopulmonary bypass. Cardiopulmonary bypass was then instituted. If the incisions involved only the right atrium, moderate hypothermia (31" to 33 C) was used. If the incisions involved the left atrium, hypothermia (25" to 28 C) was used. Under cardioplegic arrest, left atrial incisions were placed to interrupt the reentrant circuit. After the operation, the animal was weaned from cardiopulmonary bypass, and after a 30-minute period of stabilization, the electrophysiologic study was repeated and electrophysiologic data were recorded in the same manner as described above. All animals received humane care in compliance with the "Principles of Laboratory Animal Care" formulated by the National Society for Medical Research, the "Guide for the Care and Use of Laboratory Animals" prepared by the National Academy of Science and published by the National Institutes of Health (NIH publication 85-23, revised 1985). In addition, the study protocol was approved by the Washington University Animal Studies Committee. Results Five months after creation of the shunt, all 10 animals exhibited atrial enlargement and hypertrophy and were inducible into sustained atrial flutter. The reentrant circuit

3 1993;56:33742 YAMAUCHI ET AL 339 OPETION FOR ATRIAL FLUTTER PRE OPETIVE FLUTTER POST OPETIW: FLUTTER Fig 2. Activation sequence maps of a single cycle of the preoperative (left panel) and postoperative (right panel) flutter are illustrated on a twodimensional (left portion of each panel) and three-dimensional (right portion of panel) representation of the atria. The two-dimensional view shows the atria unfolded with the anterior view of the atria above and the posterior view of the atria below. The three-dimensional representation is a posterior-superior view with a portion of the pulmonary veins removed to visualize the atrial septum. The preoperative map shows a reentrant circuit (black arrows) rotating around the superior vena cava (SVC), a line of functional block (thick black line), and the right atrial appendage. After placement of an incision from the SVC to the inferior vena cava (IVC), flutter recurred with the circuit rotating around the right atrial appendage and a line of functional block. The hatched line represents the suture line used to close the incision. (Abbreviations are as in Figure 1.) was in the right atrium in 7 of the 10 dogs. The right atrial circuit could rotate clockwise or counterclockwise, and in 6 of the 7 animals, the circuit involved an anatomic orifice (superior vena cava, inferior vena cava, right atrial appendage, or a combination of these). One animal exhibited a reentrant circuit rotating around a line of functional block on the posterior right atrium. Three animals had their reentrant circuit located in the left atrium. All three of these involved the pulmonary veins. In 1 of these animals, the left atrial appendage was also involved in the circuit. The cycle length of the flutter ranged from 120 to 150 milliseconds. Initially, an attempt was made to place the minimum number of incisions needed to block the reentrant circuit. An example is shown in Figure 2. In that figure, the preoperative map during flutter demonstrated a reentrant circuit rotating in a counterclockwise direction (viewed posteriorly) around the superior vena cava and right atrial appendage. To interrupt this reentrant circuit, a longitudinal incision extending from the superior to inferior vena cava was placed just lateral to the crista terminalis, avoiding the sinus node region. Postoperatively, atrial flutter could be reinduced. Mapping revealed that there was a new reentrant circuit on the right atrium that encircled the right atrial appendage, combined with a region of functional block on the posterior right atrium. A second animal, which also had a right reentrant circuit, also had development of right atrial flutter postoperatively. Subsequently, it was decided that when a reentrant circuit was found in the right atrium, a more extensive set of right atrial incisions would be made that would eliminate not only the anatomic substrate for the reentrant circuit responsible for the atrial flutter, but potential substrates for reentrant circuits in the right atrium. Because flutter circuits usually rotated around anatomic obstacles, the surgical incisions were designed to preclude this type of reentry. This involved a longitudinal incision extending from the superior to inferior vena cava, placed just lateral to the crista terminalis to preserve sinus node function. A free-wall incision extending from the longitudinal incision to the level of the tricuspid annulus was made, and a cryolesion was placed at the annulus. Finally, the right atrial appendage was removed, a third incision was made extending from the right atrial appendage to the tricuspid valve annulus, and a second cryolesion was placed at this point. An example of this is shown in Figure 3. Preoperative mapping demonstrated a right atrial free-wall reentrant loop rotating in a counterclockwise direction. The more extensive atrial incisions were made (see Fig 3, right panel), and the flutter was no longer reinducible. When the reentrant circuit was located in the left atrium, the following incisions were placed. First, the pulmonary veins were isolated from the left atrial free wall. Then, a longitudinal incision extending from the pulmonary vein isolation to the level of the mitral annulus was made and a cryolesion was placed at the mitral valve annulus. Finally, the left atrial appendage was removed, a third incision was made extending from the atrial appendage to the level of the mitral annulus, and a second cryolesion was placed. In Figure 4, an example of a left atrial reentrant circuit that rotates in a clockwise direction around the pulmonary vein and left atrial appendage is shown. The left atrial incisions, as described above, were placed (see Fig 4, right panel), and the flutter was no longer inducible. This surgical strategy was repeated in animals 3 through 8. In all 6 animals, the incisions ablated

4 340 YAMAUCHI ET AL OPETION FOR ATRIAL FLUTTER 1993; Fig 3. A single reentrant circuit that rotated around a line of functional block on the posterior right atrium (left panel) was ablated by the more extensive right atrial incisions (right panel). See text for further details. (Abbreviations are as in Figure 1.) the reentrant circuit in the atrium in which they were made. However, in 3 of the 6 animals, flutter developed in the contralateral atrium. An example of this is shown in Figure 5, in which a reentrant circuit mapped preoperatively rotated around the pulmonary veins in a counterclockwise direction. The left atrial incisions illustrated in the right panel were made, but postoperatively, flutter was reinducible and mapping revealed that the circuit was now on the right atrium, with the circuit rotating around the superior vena cava and a line of functional block in a clockwise direction. Because of the high (50%) recurrence rate of flutter with this approach, the last two studies were performed with a combined approach in which both the left atrial incisions illustrated in Figures 4 and 5 were used, combined with the incisions illustrated in Figure 3. These biatrial incisions prevented recurrence of atrial PRE OPETIVE flutter in both animals. The results for all 10 animals are summarized in Table 1. Comment The flutter induced in this model of atrial enlargement and hypertrophy was characterized by macroreentrant loops in either the left and right atrium that generally circulated around anatomic orifices such as the superior and inferior venae cavae, pulmonary veins, and the right and left atrial appendages. The demonstration of macroreentry as the underlying mechanism for flutter is consistent with other animal and human studies [l-81. On the surface, it would appear that these large, stable, macroreentrant loops would be amenable to surgical interruption. However, there are few reports of attempts E-NO F Fig 4. A left atrial circuit that rotates around the left pulmonary veins and left atrial appendage (left panel) was ablated by the incisions shown in the right panel. See text for further details. (Abbreviations are as in Figure 1.)

5 _l l 1993;56:33742 YAMAUCHI ET AL 341 OPETION FOR ATRIAL FLU'ITER PRE OPETIVE FLUTTER POST OPETIVE FLUTTER -- I-- I Fig 5. A left atrial circuit that rotated around the pulmonary veins (left panel) undenvent the same ablative procedure shown in Figure 4. Postoperatively (right panel), a right atrial circuit that rotated around the superior vena cava (SVO and a line of functional block could be induced. See text for further details. (Abbreviations are as in Figure 1.) to surgically ablate atrial flutter. Guiraudon and associates [9] reported 3 cases of operative therapy for atrial flutter. Intraoperative mapping in the patients demonstrated a macroreentrant circuit with an area of slow conduction in the inferior atrial septum between the coronary sinus and tricuspid valve. Cryoablation of this region terminated the flutter. However, subsequently, symptomatic atrial fibrillation developed in 1 patient. In another patient reported by Canavan and associates [lo], atrial flutter in the posterior right atrium secondary to an atriotomy made previously to correct a secundum atrial septal defect was demonstrated by intraoperative mapping. To ablate the tachycardia, a transverse incision was made across the right atrial reentrant circuit. The incision extended from the atrioventricular groove, across the right atrial free Table 1. Data Summary" Dog No Preoperative Preoperative Postoperative Circuit Circuit Ablated Circuit a A single procedure limited to one atrium ablated the flutter in 3 of 10 dogs (dogs 3, 4, and 5). In 5 of 10 dogs, a second atrial flutter circuit appeared, frequently in the opposite atrium (dogs 1, 2,6, 7, and 8). Biatrial incisions were placed initially in 2 of 10 dogs (dogs 9 and lo), with no recurrence of inducible atrial flutter. = left atrial; = right atrial. wall, to the atrial septum, through the septum, and across the anterior limbus of the fossa ovalis to the atrial septal patch. However, 1 month later, flutter developed again. Similar results have been obtained in studies in which catheter ablation of flutter was attempted [ll]. In the study by Saoudi and associates [ll] involving 8 patients, 1 had a recurrence of flutter and 3 had intermittent fibrillation. The present study demonstrates a potential mechanism behind the high recurrence rates. The data suggest that in this model of flutter, there are multiple potential reentrant circuits. When the flutter is induced, the most stable of these will dominate, passively activating the remainder of the atrium in a 1:l fashion. As illustrated in Figure 2, a minimal operation to interrupt a specific pathway resulted in another right atrial reentrant pathway. Subsequently, incisions were developed that removed the potential reentrant pathways observed in the right atrium (see Fig 3) and left atrium (see Figs 4, 5). These right and left atrial incisions were designed to prevent any reentrant circuits from rotating around anatomic orifices, such as the cavae, appendages, or pulmonary veins. Incisions on the right posterior free wall carried to the tricuspid valve, prevented rotation of a circuit around the tricuspid valve orifice, and also at the same time prevented the reentrant circuit from rotating around a line of functional block in the posterior right free wall, which is the site where the circuits usually occur. The incisions on the left, carried to the mitral valve annulus, prevented rotation of the reentrant circuit around the mitral valve orifice. However, with placement of only the left or only the right incisions, there was a high recurrence rate of 50% with the new reentrant circuit appearing in the contralateral atrium. Combining both the left atrial and right atrial incisions resulted in no recurrences of the flutter. The combined biatrial incisions are similar to those developed in our

6 342 YAMAUCHI ET AL OPETION FOR ATRIAL FLUTTER 1993:56:33742 Fig 6. An anatomic drawing of the biatrial incision used to prevent the inducibility of atrial flutter is shown in the right panel. On the left is an illustration of the original maze procedure used to ablate atrial jibrillation. The hatched line represents the suture line used to close the incisions. laboratory to treat atrial fibrillation [12, 131 (Fig 6). This similarity supports the concept that atrial flutter and fibrillation may have common underlying arrhythmogenic substrates [5]. The specific etiology of atrial flutter in humans is unknown. Therefore, both drug and surgical therapies tested in animal models of flutter may not be directly applicable to human flutter. Only when the underlying substrates for flutter are determined will it be possible to define the optimum procedure. Even the biatrial incision used in this study would have to be tested om an extensive number of animals to prove that it is the optimum procedure in this animal model. However, the results of this study suggest that ablative therapies based on a limited dissection, cryoablation, or electrical ablation can fail to remove all the underlying substrates for flutter and may risk a high recurrence rate. This is consistent with the limited number of clinical studies already reported and provides a potential explanation for failiires of these procedures. More extensive atrial operations, such as the biatrial incisions used in this study or the procedure used for the treatment of atrial fibrillation, may be necessary for the treatment of atrial flutter in which there is a substrate for multiple reentrant pathways. Supported by National Institutes of Health grants R01 HL33722 and R01 HL References 1. Klein GJ, Guiraudon GM, Sharma AD, Milstein S. Demonstration of macroreentry and feasibility of operative therapy in the common type of atrial flutter. Am J Cardiol 1986; Chang BC, Schuessler RB, Stone CM, et al. Computerized mapping of the atrial septum in patients with atrial flutter. Circulation 1989;8O(Suppl 2): Cosio FG, Arribas F, Palacios J, Tascon J, Lopez GM. Fragmented electrograms and continuous electrical activity in atrial flutter. Am J Cardiol 1986; Boineau JP, Schuessler RB, Mooney CR, et al. Natural and evoked atrial flutter due to circus movement in dogs. Am J Cardiol 1980;45: Cox JL, Canavan TE, Schuessler RB, et al. The surgical treatment of atrial fibrillation: 11. Intraoperative electrophysiologic mapping and description of the electrophysiologic basis of atrial flutter and atrial fibrillation. J Thorac Cardiovasc Surg 1991;101: Boyden PA. Activation sequence during atrial flutter in dogs with surgically induced right atrial enlargement. I. Observation during sustained rhythms. Circ Res 1988;62: Page PL, Plumb VJ, Okumura K, Waldo AL. A new animal model of atrial flutter. J Am Coll Cardiol 1986;8: Yamauchi S, Sato S, Schuessler RB, Boineau JP, Matsunaga Y, Cox JL. Induced atrial arrhythmias in a canine model of left atrial enlargement [Abstract]. PACE 1990;13: Guiraudon GM, Klein GJ, Sharma AD, Yee R. Surgical alternatives for supraventricular tachycardias. In: Touboul P, Waldo AL, eds. Atrial arrhythmias: current concepts and management. St. Louis: Mosby-Year Book, 1990;48% Canavan TE, Schuessler RB, Cain ME, et al. Computerized global electrophysiological mapping of the atrium in a patient with multiple supraventricular tachyarrhythmias. Ann Thorac Surg 1988;46: Saoudi N, Atallah G, Kirkorian G, Touboul 1. Catheter ablation of the atrial myocardium in human type I atrial flutter. Circulation 1990;81: Cox JL, Schuessler RB, DAgostino HJ Jr, et al. The surgical treatment of atrial fibrillation: 111. Development of a definitive surgical procedure. J Thorac Cardiovasc Surg 1991;lOl: Cox JL. The surgical treatment of atrial fibrillation: IV. Surgical technique. J Thorac Cardiovasc Surg 1991;lOl: