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J Thorac Cardiovasc Surg 1996;111:514-526
© 1996 Mosby, Inc.
SURGERY FOR CONGENITAL HEART DISEASE |
Supported by National Institutes of Health grants HL32257 and HL33722. Dr. Rodefeld was supported by a National Research Service Award Grant (HL08894).
Address for reprints: Charles B Huddleston, MD, Department of Surgery, Division of Cardiothoracic Surgery, Box 8234, 3308 Queeny Tower, One Barnes Hospital Plaza, St. Lous, MO 63110.
Abstract
Intraatrial reentrant tachycardia, or atrial flutter, is a common postoperative problem after Fontan repair, which involves an atriopulmonary connection. A modification of Fontan repair, total cavopulmonary connection, minimizes the portion of the right atrium exposed to stretch and hypertension; however, atrial flutter continues to occur after this procedure. We postulated that the intraatrial lateral tunnel suture line of total cavopulmonary connection, in the absence of physiologic alterations such as atrial hypertension or stretch, provides the necessary electrophysiologic substrate for atrial flutter. The purpose of this study was to produce a canine model of total cavopulmonary connection (1) to establish that the intraatrial suture line alone is sufficient to permit sustained atrial flutter and (2) to characterize the pathways of resulting reentrant arrhythmias. After induction of general anesthesia, 25 to 30 kg dogs (n = 17) underwent median sternotomy, cradling of the pericardium, and placement of a pacing electrode on the right atrial appendage. Normothermic cardiopulmonary bypass was initiated. The total cavopulmonary connection suture line was placed through a standard right atriotomy, simulating construction of the lateral tunnel. After closure of the atriotomy, 253 point unipolar atrial endocardial form-fitting electrodes were placed through bilateral ventriculotomies. By means of atrial burst pacing and programmed extrastimulation, induction of atrial flutter was attempted. If atrial flutter could not be induced, isoproterenol was infused and the stimulation protocol was repeated. After induction of atrial flutter, mapping of the activation sequence was performed. Before suture line placement, no dog had inducible atrial flutter. After placement of the suture line, sustained atrial flutter was reproducibly induced in every dog, although isoproterenol was required for this in three (17.6%). The mean flutter cycle length was 177 ± 30 msec. In each case, the atrial flutter circuit was limited to the right atrium, with the left atrium being passively activated. The atrial flutter circuit was dependent on a corridor of myocardium that resulted from conduction block on the free wall, created by the lateral margin of the total cavopulmonary connection. In no case was the atriotomy integral to the atrial flutter circuit. This study establishes that the total cavopulmonary connection baffle suture line alone, without alteration in circulatory physiology, creates a sufficient anatomic substrate for atrial flutter in a short-term canine model. Delineation of the anatomic boundaries of the reentrant circuit raises the possibility of targeting areas within the circuit that could be modified, potentially reducing the incidence of postoperative atrial flutter after total cavopulmonary connection. (J THORAC CARDIOVASC SURG 1996;111:514-26)
Intraatrial reentrant tachycardia, or atrial flutter (AFL), results in substantial morbidity among patients who have undergone the Fontan operation.
1-3 Supraventricular tachycardia is poorly tolerated by patients with single-ventricle physiology. Pharmacologic treatment is often ineffective and may be complicated by the proarrhythmic and negative inotropic properties of antiarrhythmic drugs.
Clinical studies suggest that right atrial hypertension may be a risk factor for both early and late arrhythmias after classic Fontan repair. 4 This operation uses an atriopulmonary connection that leads to extreme dilatation as well as to elevated pressure in the entire right atrium. Total cavopulmonary connection (TCPC) is a recent modification of the Fontan procedure in which a C-shaped lateral tunnel, or baffle, is used to direct blood from the inferior vena cava through the right atrium to the pulmonary artery. 5 It was anticipated that the TCPC would reduce the incidence of postoperative AFL because only a small portion of the right atrium is exposed to stretch and hypertension. 6 Intermediate follow-up to 5 years, however, indicates that tachyarrhythmias after the TCPC continue to be a problem, ranging in frequency from 4% to 35%. 4,7,8 We therefore hypothesized that the lateral tunnel suture line alone, in the absence of changes in circulatory physiology, establishes an anatomic substrate for AFL. The objectives of this study were as follows: (1) to determine whether the lateral tunnel suture line alone is sufficient to permit sustained AFL and (2) to characterize the pathways of resultant arrhythmias.
Methods
Operation
Adult mongrel dogs weighing 25 to 30 kg (n = 17) were anesthetized with intravenous pentobarbital sodium (30 mg/kg), intubated with a cuffed endotracheal tube, and mechanically ventilated with a volume-cycled ventilator. An adequate level of anesthesia was maintained by intermittent infusion of 1 to 2 mg pentobarbital sodium. Limb-lead electrocardiography was monitored, and a 20-gauge arterial pressure catheter was placed in the left femoral artery. After median sternotomy, the azygous vein was ligated and the heart cradled in the pericardium. Bipolar pacing and sensing electrodes were sutured to the right and left atrial appendages, respectively. After systemic heparinization (1 mg/kg), a 16F arterial cannula was placed into the right femoral artery and bicaval venous cannulation was performed with 28F venous cannulas positioned as far as possible away from the right atrium. Normothermic cardiopulmonary bypass was instituted; to avoid acute changes in postoperative atrial refractoriness, cardioplegic arrest was not used. A standard longitudinal right atriotomy was made from the midatrial appendage, anterior to the crista terminalis, to the level of the sinus node artery in the lower right atrial free wall. Care was taken to avoid disruption of the sinus node artery, which arises from the distal right coronary artery in 95% of dogs.
A continuous 4-0 polypropylene suture was then placed inside the right atrium in a manner simulating lateral tunnel construction in TCPC; no baffle was placed. The suture line started at the limbus of the fossa ovalis and traveled inferiorly, lateral to the fossa ovalis, between the coronary sinus and the inferior vena caval orifice, around the inferior vena cava, laterally up the crista terminalis, around the superior vena caval orifice, and back to the limbus of the fossa ovalis (Fig. 1, A). The atriotomy was then closed with a continuous 4-0 polypropylene suture.
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Atrial burst pacing at cycle lengths of 200 to 400 msec was performed before and after the atriotomy. After the TCPC suture line was placed and the intraatrial electrodes were implanted, the cycle length of the atrial burst pacing was shortened to 110 to 250 ms. In six dogs, single atrial premature stimuli were delivered after an 8-beat drive train of 200 to 250 msec. When sustained AFL could not be induced, a 0.3 µg/kg bolus of isoproterenol was injected into the cardiopulmonary bypass circuit and the pacing protocol was repeated.
Sustained AFL was defined as a fixed cycle length tachycardia of greater than 30 seconds in duration. Reproducibility was determined by reinduction of the tachyarrhythmia with the same extrastimulus pattern that had originally induced it.
Data acquisition and analysis
Atrial activation sequence data were obtained by simultaneously recording 253 unipolar electrograms from the endocardial multipoint electrodes. Limb-lead electrocardiograms and bipolar atrial electrograms from either the right or left atrial appendage were also simultaneously recorded. Data were recorded during spontaneous rhythm and during any sustained arrhythmia with a 256-channel computerized data-acquisition and data-analysis system based on a VaxStation II/GPX graphics workstation connected to two 128-channel PDP 11/23+–based data-acquisition subsystems (Digital Equipment Corporation, Maynard, Mass.). The system is run with in house–developed software (GLAS) for data acquisition control, management, display, and analysis. Unipolar electrograms were recorded at a gain of 1000 with a frequency response of 50 to 500 Hz. Each channel was digitized at 1000 Hz with a 12-bit resolution. Local endocardial activation times were determined from the time of the maximum negative derivative (-dV/dt) of the unipolar electrogram. All electrograms were edited visually to verify accuracy of computer-selected activation times. Computer-generated activation sequence maps were reconstructed from all recordings. Data processing and three-dimensional interactive display was performed on a Silicon Graphics Iris 4D/320GTX high-performance graphic workstation (Silicon Graphics Inc., Mountain View, Calif.). Activation sequence maps were displayed as real-time three-dimensional movie images on a three-dimensional surface model of the canine atrium. 9
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 Academy of Science and published by the National Institutes of Health (NIH Publication 86-23, revised 1985). In addition, the study protocol was approved by the Washington University Animal Studies Committee.
Results
AFL could not be induced in any case either before or after atriotomy alone. Although rapid atrial burst pacing was often required to induce AFL after placement of the lateral tunnel suture line, when done before or after atriotomy alone paced cycle lengths less than 150 msec typically induced either atrial fibrillation or an extremely rapid tachycardia (cycle length 
120 msec). Consequently, to minimize the need for direct current cardioversion, atrial burst pacing at cycle lengths less than 200 msec was not attempted in later studies until after the suture line was in place.
AFL was reproducibly induced in 14 of 17 animals (82%) after placement of the lateral tunnel suture line (Table I), with a mean cycle length of 173 ± 30 msec. In the three remaining dogs, after isoproterenol was administered AFL was induced with a mean cycle length of 194 ± 33 msec (Table I). The tachycardias induced met the conventional clinical criteria for AFL. They could be pace induced and pace terminated, and they exhibited a fixed cycle length that was not dependent on participation of the ventricle (Fig. 2). The presence of reentry within the atrium was confirmed by atrial activation sequence maps, which demonstrated continuous electrical activity throughout the entire tachycardia cycle length (Fig. 3).
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The line of block on the free wall was anatomic rather than functional, as evidenced by its persistence during sinus rhythm (Fig. 4). Earliest activation occurred in the intercaval region of the free wall, near the sinus node. As the wave front propagated from the region of the sinus node, it encountered a zone of block corresponding to the site of the suture line along the crista terminalis. In the example shown, the block was not complete; time isochrones demonstrate a breakthrough in the rostral section. The block is sufficient, however, to result in delayed activation of the corridor between the suture line and the tricuspid anulus. This corridor is activated by wave fronts that travel posteriorly around the inferior and superior venae cavae, where they cross over the suture lines and return onto the free wall. As it is during AFL, conduction along the septum is rapid, uniform, and unaltered by the lateral tunnel suture line.
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Despite initial optimism that TCPC would lessen the incidence of postoperative atrial tachyarrhythmias in patients with single ventricle physiology, such a reduction has not consistently been observed. Even in the most favorable studies, the incidence of atrial tachyarrhythmias remains 4%. 8 Furthermore, follow-up periods have been short, less than 5 years. Extrapolating from the experience after operations for other types of congenital heart disease, particularly Mustard repair for transposition of the great arteries, the incidence of atrial arrhythmias may be expected to increase for years after the operation. 10
Minimum substrate for AFL
The determinants of human AFL after TCPC are poorly understood. Clinical studies have implicated functional block in human AFL, 11,12 and a recent study demonstrated functional block related to the crista terminalis and eustachian ridge. 13 Animal models of AFL have demonstrated functional components that may be related to a variety of factors, including atrial distention and fibrosis. 14,15 Atrial hypertension has also been implicated in human beings. 4,16 The results of this study demonstrate that in the short term, however, the anatomic barrier imposed by the suture line alone in TCPC is sufficient to permit sustained AFL. The study design avoided alterations in atrial physiology inherent in the TCPC operation by using a suture line without the baffle, eliminating the confounding variables of atrial stretch and hypertension.
The segment of the TCPC line on the free wall consistently produced a line of block during both sinus rhythm and AFL. The isthmus of myocardium between this surgical line of block and the naturally occurring barrier of the tricuspid anulus was critical to perpetuating the tachycardia. The suture line on the free wall protected this isthmus from competing wave fronts in a manner similar to the Y-incision described by Frame and coworkers. 17,18 No pathologic zones of slow conduction were required. Viewed differently, the line of block prevented the wave front within this zone from exiting at sites other than at the caudal or rostral margins of the free wall. This created a sufficiently long reentry circuit that the myocytes within this zone were once again excitable by the time the wave front exited one end of this corridor and returned to the other end.
In contrast to the portion of the suture line on the free wall, the TCPC segment of the suture line on the septal side did not appear to affect conduction. This may be related to anatomic differences in the two surfaces. The suture line on the free wall was created with full-thickness bites, whereas those on the septal surface were not. Previous studies from this laboratory have demonstrated that the right and left sides of the atrial septum are functionally and anatomically separate over most of their distribution. 19 There are discrete regions of communicating myocyte bundles, however, which may have provided a mechanism by which impulses traveled along the septum in a uniform fashion despite the sutures. Impulses could have crossed over to the left side of the septum at the caudal margin, propagated up the unaffected left atrial component of the septum, and then crossed again to the right atrial component.
Potential for multiple reentry circuits
One of the puzzling aspects of clinical AFL in patients with Fontan physiology is the presence of apparent multiple reentry circuits, as determined by variable cycle lengths and differing P-wave morphologic patterns on the surface electrocardiogram. It is not uncommon in patients with AFL to see two or three different cycle lengths, each with a different P-wave morphologic pattern. The findings from this model suggest two mechanisms by which this may happen. Clockwise and counterclockwise loops were equally prevalent in the dogs studied. Although we did not observe examples of circus movement tachycardia in opposite directions in the same dog, it seems likely that this would occur clinically. This would result in different P-wave morphologic patterns and, depending on whether conduction velocity is affected by the direction of the wave front, possibly a change in cycle length. A second way that this might happen is illustrated by the dog who exhibited at least three different routes by which the impulse could rotate around the suture line on the free wall (Fig. 5). Each route would presumably produce a different cycle length and a different P-wave morphologic pattern. Regardless of the potential for multiple circuits in any single dog, however, the AFL in all cases had in common a dependence of the protected isthmus on the free wall created by the lateral tunnel suture line.
Role of functional block
Macroreentrant tachycardias such as AFL require not only an electrophysiologic substrate but a trigger as well. One of the characteristics of atrial tachyarrhythmias after Fontan repair is the progressive increase in frequency with time. If the electrophysiologic substrate for AFL is an anatomic barrier present from the time of operation, other factors must be operative to explain late onset. One factor that might change with time and thus further predispose a patient toward the development of AFL is the extent of functional block. In an example of AFL initiated by an atrial premature beat, unidirectional block was responsible for initiating the tachycardia (Fig. 6). This unidirectional block was functional, occurring in a portion of the atrium unrelated to surgical or naturally occurring barriers. There are multiple potential explanations for increasing functional block with time, including diminished conduction safety margin, changes in gap junction function, and alterations in autonomic tone. Perhaps the most likely cause of functional block in this setting is an increase in dispersion of refractoriness. For example, progressive fibrosis may increase the probability of functional unidirectional block. If the frequency of atrial premature beats rises with time, the probability of an ill-timed event that initiates reentry is further increased. Alterations in the trigger for AFL may therefore account for the clinically observed late onset of arrhythmias.
Comparison of TCPC with previous models of AFL
Previous surgical models of AFL share common features with our TCPC model. In the classic study of Rosenblueth and Garcia Ramos, 20 a crush injury in the intercaval region resulted in sustained and reproducible AFL circulating around both caval orifices (Fig. 7, A). Subsequent animal models of AFL have supported these findings. 21,22 More recently, Frame and coworkers 17,18 described a modification of the intercaval crush model in which a Y-shaped spur incision was extended from the intercaval lesion to the right atrial appendage (Fig. 7, B). The spur incision forced the reentrant circuit to rotate instead around the tricuspid anulus. A canine model of AFL after Mustard repair showed a similar circuit involving the tricuspid anulus, although the role of anatomic barriers in this operation is much more complicated than in other models. 23
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20 or around the tricuspid anulus, as in the model of Frame and coworkers 17,18 (Fig. 7, C). In reality, the reentry circuit is not a line, as it is often portrayed in schematic diagrams, but rather a band of tissue. In the case of TCPC, the critical isthmus is bounded on one side by the superior and inferior venae cavae linked by a suture line and on the other side by the tricuspid anulus. The reentrant circuit exists between two barriers, the free wall TCPC suture line and the tricuspid anulus.
Implications
Successful catheter ablation of human type I AFL has been achieved. 24,25 This success resulted from an understanding of the critical role of the isthmus of tissue between the tricuspid anulus and the inferior vena cava. Experience with catheter ablation of AFL after operations for congenital heart defects has been limited, and results have varied. 26,27 We believe that consideration of the anatomy specific to each type of operation for congenital heart defects is important in the understanding potential reentrant circuits. With regard to TCPC, interruption of the corridor between the lateral tunnel suture line and the tricuspid anulus may be the key to eliminating AFL after operation.
Limitations of the study
The animal model used in this study had normal cardiac anatomy. It is possible that atrial abnormalities commonly found in children with single-ventricle physiology would result in conduction properties different from those of normal atria. The AFL circuits observed in this study were induced by pacing. It is possible that induced AFL might not be identical to tachycardias that occur spontaneously. Also, whether the AFL seen in the short term would remain inducible in the long term and whether it would involve a similar reentry circuit is unknown. Finally, by necessity, mapping of AFL took place after insertion of the intraatrial electrodes. The AFL may therefore have been affected by stretch or endocardial injury caused by these electrodes.
Conclusion
A canine model of acute AFL after the modified Fontan operation is described. The lateral tunnel suture line in TCPC construction has been demonstrated to be sufficient to create an anatomic substrate for the development and maintenance of a single distinct AFL pathway that revolves in the right atrium primarily around the venae cavae. An understanding of the anatomic constituents of AFL circuits in this model will help facilitate the future development of treatment strategies for patients undergoing the modified Fontan procedure.
Appendix: Discussion
Dr. Richard A. Jonas (Boston, Mass.)
Dr. Rodefeld and his group invited me to comment on this presentation. I congratulate him on the presentation and congratulate the group for this fascinating study. I think the videos are absolutely spectacular.
I am not an electrophysiologist, but our group does have extensive experience with the Fontan procedure for complex single ventricle. The significance of this study is the development of an animal model that may facilitate the design of a surgical technique to minimize the incidence of inducible AFL early after a modified Fontan procedure. However, continuing work remains to be done. It is important for clinical studies to be undertaken to confirm that early inducible AFL is indeed correlated with an increased risk of late atrial arrhythmias, which is the fundamental premise and implication of this presentation.
Probably several mechanisms in addition to suture load contribute to the development of atrial reentrant tachycardia or AFL late after operations. These include the number and location of both functional and anatomic holes within the atrium, including great vein ostia and surgical incisions, the presence of abnormal atrial myocardium, and elevated atrial wall stress, which is determined by both the right atrial pressure and the diameter of the right atrium in accordance with Laplace's Law. We believe that the lateral tunnel reduces atrial wall stress by reducing the diameter of the right atrial chamber. In addition, the area of right atrial wall exposed to high pressure is minimized.
In a recent analysis of 500 patients who underwent Fontan procedures at Children's Hospital in Boston between 1973 and 1991, the following factors were found to be associated with increased risk of AFL late after operation: older age at operation, sinus node dysfunction, and nonuse of the lateral tunnel. The absence of sinus rhythm at the time of the Fontan procedure was a powerful predictor for subsequent development of AFL.
The late follow-up of our patients who have undergone the Fontan procedure suggests that the lateral tunnel approach may be associated with a reduced late incidence of atrial arrhythmias related to the use of an extracardiac conduit or an atriopulmonary anastomosis. Follow-up is too short as yet to be sure of this.
I have two questions. First, have you compared the lateral tunnel suture line with alternative suture lines, such as the oblique baffle suture line that encircled the tricuspid anulus and excised atrial septum, which we used for patients with left atrioventricular valve atresia? Clinically, this procedure appears to have been accompanied by a higher incidence of late atrial arrhythmias, and perhaps some implications of the early findings could be correlated with the late clinical findings that we already have. Second, I ask you to expand on the methods by which you would reduce the risk of AFL with the lateral tunnel approach or to speculate regarding completely novel methods that could reduce the incidence of late arrhythmias.
Dr. Rodefeld
In response to your first question, we have not looked at alternative suture line placement or baffle construction. This model was developed purely for the study of AFL after classic TCPC lateral tunnel suture line placement.
In response to your second question regarding methods to reduce the risk of AFL occurring after TCPC construction, there appear to be two potential means by which the probability of AFL can be reduced. The first, as mentioned in the presentation, is to produce a line of conduction block between the two boundaries within which the reentrant pathway conducts. This could be performed either surgically or transvenously with a cryolesion or radiofrequency ablation. The second possible alternative would be to modify the TCPC suture line in some way to try to avoid the conduction block that we have observed along the crista terminalis. If the suture line could be moved away from the crista either medially or laterally, the incidence of AFL might be reduced. Further experimental studies would be required to determine whether this would actually reduce the incidence of AFL.
Dr. Jonas
To create this block between the suture line and the tricuspid anulus, would you place a cryoprobe from the suture line inferior to the coronary sinus and just across to the tricuspid anulus?
Dr. Rodefeld
Theoretically, yes. Any nonconductive lesion between those two barriers should ablate the arrhythmia. Because the AFL pathway that we observed is narrowest in the lower right atrium, where it comes around the inferior vena cava near the tricuspid anulus, this would be a likely site for ablative therapy.
Dr. Gerhard Ziemer (Tübingen, Germany)
For reasons other than avoiding possible arrhythmias—avoidance of patch leaks and to speed up the procedure by simplification—in the last 50 of our 70 patients in whom a so-called "lateral tunnel" was performed we did not create the tunnel within the right atrium with the atriotomy still open. Instead, we used the lateral patch suture line to also close the atriotomy by sandwiching the patch within the rims of the atriotomy. By this procedure, we clearly do not create any isolated lateral suture lines other than for the atriotomy.
In fact, looking at our whole series of 90 patients who have undergone the Fontan procedure and doing electrophysiologic studies on them, we discovered that about 90% of the patients with lateral tunnels chiefly constructed in this way had sinus rhythm about 2
after the operation, whereas only 60% of the patients who underwent so-called more classic atriopulmonary anastomoses reveled stable sinus rhythm.
In this aspect, the lateral tunnel seems to be advantageous. After listening to your presentation, we may go back and look to see whether we can find a difference between the classic lateral tunnels and those for which, purely by accident, we may have performed an antiarrhythmic modified Fontan procedure.
Dr. Marshall L. Jacobs (Philadelphia, Pa.)
I enjoyed your elegant model immensely and, like my colleague Dr. Ziemer, I found that your experiment has shed some light on what was probably a fortuitous situation with our patients in Philadelphia who underwent the Fontan procedure. Having performed more than 300 lateral tunnel TCPCs, it has routinely been the case that the medial aspect of the baffle or tunnel has been sutured in a fashion similar to what you showed in your experiments, but the lateral baffle aspect, as described by Dr. Ziemer, was incorporated directly into the closure of the atriotomy, which was routinely made approximately 1 cm anterior to and parallel to the crista terminalis. We have not routinely subjected these patients to electrophysiologic studies, but the incidence of spontaneous as opposed to inducible AFL in that population has anecdotally been very, very low. I was fascinated by the absence of the contribution of the atriotomy to the pathology in your model, and like Dr. Ziemer I wonder whether incorporating the suture line into the atriotomy parallel to and away from crista terminalis may represent a potential solution to this problem.
Dr. Rodefeld
I agree that this is a very interesting clinical observation, and I think that this question can really only be answered by further electrophysiologic mapping studies. It is interesting to note that injury to the crista terminalis is a common theme in many animal models of AFL, and the idea that impairment of longitudinal conduction in the crista terminalis may predispose toward reentry is intriguing and deserves further investigation.
Acknowledgments
We thank Donna Marquart, Tim Morris, Duane Probst, and Dennis Gordon for their expert technical assistance.
Footnotes
From the Division of Cardiothoracic Surgery, Department of Surgery,a and Division of Pediatric Cardiology, Department of Pediatrics,b Washington University School of Medicine, St. Louis, Mo. 
Read at the Seventy-fifth Annual Meeting of The American Association for Thoracic Surgery, Boston, Mass., April 23-26, 1995.
J THORAC CARDIOVASC SURG 1996;111:514-26
References
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D. A. Vitullo, S. Y. DeLeon, T. E. Berry, J. J. Bonilla, S. V. Chhangani, F. Cetta, J. A. Quinones, T. J. Bell, and E. A. Fisher Clinical Improvement After Revision in Fontan Patients Ann. Thorac. Surg., June 1, 1996; 61(6): 1797 - 1804. [Abstract] [Full Text]
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S. K. Gandhi, B. I. Bromberg, and C. B. Huddleston Surgical technique and atrial arrhythmias after total cavopulmonary connection J. Thorac. Cardiovasc. Surg., June 1, 1996; 111(6): 1291 - 1292. [Full Text]
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S. K. Gandhi, B. I. Bromberg, M. D. Rodefeld, R. B. Schuessler, J. P. Boineau, J. L. Cox, and C. B. Huddleston Lateral Tunnel Suture Line Variation Reduces Atrial Flutter After the Modified Fontan Operation Ann. Thorac. Surg., May 1, 1996; 61(5): 1299 - 1309. [Abstract] [Full Text]
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