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Ann Thorac Surg 1996;61:1299-1309
© 1996 The Society of Thoracic Surgeons
Division of Cardiothoracic Surgery, Department of Surgery, and Division of Pediatric Cardiology, Department of Pediatrics, Washington University School of Medicine, St. Louis, Missouri
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Abstract |
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 TopFootnotes Abstract IntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Methods. Adult mongrel dogs (n = 25) underwent a median sternotomy and normothermic cardiopulmonary bypass. In groups 1, 2, and 3, through a right atriotomy, a suture line was placed to simulate the lateral tunnel of the modified Fontan operation (n = 20). The lateral aspect of the suture line ran along the CT in group 1 (n = 10), 5 mm medial to the CT in group 2 (n = 5), and 10 mm anterior to the CT, incorporated into the atriotomy closure, in group 3 (n = 5). In group 4 (n = 5), only the lateral portion of the suture line, along the CT, was placed. Form-fitting 253-point unipolar endocardial mapping electrodes were inserted into the left and right atria via bilateral ventriculotomies. Induction of AFL was then attempted using atrial burst pacing. If sustained AFL could not be induced, isoproterenol was administered and the pacing protocol repeated. Endocardial activation sequence maps of spontaneous rhythm and AFL were constructed.
Results. Under baseline conditions, after placement of the suture line, sustained AFL could reproducibly be induced in 8/10 dogs in group 1, 0/5 dogs in group 2, 0/5 dogs in group 3, and 5/5 dogs in group 4 (p < 0.001). After isoproterenol administration, sustained AFL was reproducibly inducible in the remaining 2 dogs in group 1, 4/5 dogs in group 2, and 0/5 dogs in group 3 (p = 0.01). The mean cycle length of AFL was 189 ± 25 ms in group 1, 136 ± 8 ms in group 2, and 182 ± 20 ms in group 4 (p < 0.001). Atrial activation sequence maps, during sinus rhythm, demonstrated a line of conduction block along the lateral portion of the suture line in all cases in groups 1 and 4 and in only those cases in group 2 in which sustained AFL was inducible. During AFL this block facilitated unidirectional conduction, permitting propagation of the reentrant wavefront. Mean conduction velocity along the CT during sinus rhythm was 0.63 ± 0.10 m/s in group 1, 1.04 ± 0.17 m/s in group 2, 1.01 ± 0.12 m/s in group 3, and 0.44 ± 0.13 m/s in group 4 (p < 0.01).
Conclusions. In an acute canine model of the modified Fontan operation, conduction block imposed by the lateral tunnel suture line is an essential component of the AFL circuit. The inducibility of AFL is increased by suture line placement along the CT. Slow conduction, resulting from injury to the CT, promotes this increased inducibility. Avoidance of the CT may reduce the incidence of AFL in children undergoing the modified Fontan operation.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Atrial flutter (AFL), or intraatrial reentrant tachycardia, is a common early and late postoperative complication of the modified Fontan operation, or total cavopulmonary connection. Some series report a prevalence as high as 30% at 5-year follow-up [1–5]. These rhythm disturbances are not well tolerated in patients with single ventricle physiology. Their management with antiarrhythmic agents and by antitachycardia pacing is complicated and fraught with failures [6, 7].
We previously investigated the electrophysiologic consequences of the modified Fontan, which uses a C-shaped lateral tunnel or baffle through the right atrium. We demonstrated that the lateral tunnel suture line alone, in the absence of hemodynamic alterations, is a sufficient anatomic substrate for intraatrial reentry in an acute canine model [8]. The reentrant circuit revolved in the right atrium around a line of conduction block imposed by the free wall Fontan suture line in continuity with the orifices of the superior and inferior venae cavae.
The unique anatomic architecture of the right atrium, in addition to surgically created obstacles, has been suggested to be related to reentry [9–13]. Involvement of the crista terminalis (CT) has been a prominent feature of several animal models of AFL [13–15]. The CT is a thick muscle bundle oriented longitudinally in the right atrium that conducts impulses rapidly in the rostrocaudal direction. We hypothesized that injury to the CT by the lateral tunnel suture line contributes to the development of AFL after the modified Fontan repair. The objective of this study was to determine the effects of alteration of the lateral tunnel suture line, relative to the CT, on the inducibility of AFL in an acute canine model.
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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). In group 2 (n = 5), the lateral aspect of the suture line was placed 5 mm medial to the CT (Fig 1B). In group 3 (n = 5), the suture line was placed 10 mm anterior to the CT by incorporating the lateral aspect into the atriotomy closure after traveling around both caval orifices (Fig 1C). In group 4 (n = 5), a suture line was placed only along the CT from the orifice of the inferior vena cava to the orifice of the superior vena cava (Fig 1D). In groups 1, 2, and 4, the atriotomy was closed separately with a continuous 4-0 polypropylene suture.
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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). The study protocol was also approved by the Washington University Animal Studies Committee.
Pacing Protocol
Programmed extrastimulation and burst pacing were performed using a programmable pulse generator (Bloom Inc, Reading, PA). Stimulus input was set at twice pacing threshold. Atrial burst pacing was conducted at cycle lengths of 100 to 250 ms. Programmed extrastimulation was done using drive trains at cycle lengths of 200 to 300 ms with premature intervals of 100 to 200 ms. Attempts to induce AFL were made (1) after bypass alone and (2) after the intraatrial suture line had been placed, the atriotomy closed, and the mapping electrodes inserted. Sustained AFL was defined as the presence of a stable tachycardia of greater than 30 seconds in duration that exhibited a fixed atrial cycle length less than 250 ms. Termination of AFL was either by overdrive pacing or premature stimulation. Reproducibility was established by reinduction of the tachyarrhythmia using the same extrastimulus pattern with which it was originally induced. In instances in which sustained AFL was not inducible, isoproterenol (3 to 6 µg/kg) was administered and the pacing protocol repeated.
Data Acquisition and Analysis
Atrial activation sequence data during spontaneous rhythm and sustained arrhythmias were obtained by simultaneously recording 253 unipolar electrograms from the endocardial multipoint electrodes. Limb lead electrocardiogram and a bipolar left atrial electrogram were recorded simultaneously. Data were recorded using a 256-channel computerized data acquisition and analysis system based on a VaxStation II/GPX graphics workstation (Digital Equipment Corp, Maynard, MA) connected to two 128-channel PDP 11/23+-based data acquisition subsystems. The system is run with in-house-developed software (GLAS). Unipolar electrograms were recorded at a gain of 1,000 with a frequency response of 50 to 500 Hz. Each channel was digitized at 1,000 Hz with a 12-bit resolution. Endocardial activation times were determined from the time of the maximum negative derivative of the unipolar electrogram. 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, CA). Activation sequence maps were displayed as real-time images on a three-dimensional surface model of the canine atria [16]. From these images, two-dimensional isochronous maps were created using previously established criteria [17]. Longitudinal conduction velocity along the CT was calculated by determining the differences in activation times of electrode points located at the superior and inferior margins of the CT.
Statistical Analysis
All values for each group are expressed as mean ± standard deviation. Statistical significance of all paired data was determined by Student's paired t test (SYSTAT 5.0; SYSTAT Inc, Evanston, IL). Data with three or more groups were compared using analysis of variance and Tukey's multiple comparisons. Differences in the inducibility of AFL between groups were assessed using 
2 analyses. A p value less than 0.05 was considered statistically significant.
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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). In group 1, in which the lateral segment of the suture line was placed along the CT, sustained AFL was reproducibly induced in 8 of 10 dogs. When the free wall portion of the suture line was moved 5 mm medial to the CT (group 2), AFL was induced in 0 of 5 dogs. Incorporation of the lateral aspect of the suture line into the closure of the atriotomy (group 3) resulted in 0 of 5 dogs having inducible AFL. In group 4, where only the free wall portion of the suture line along the CT was placed, AFL was inducible in 5 of 5 dogs. After the administration of isoproterenol, sustained AFL was reproducibly induced in the remaining 2 dogs in group 1 and 4 of 5 dogs in group 2. However, even with isoproterenol, AFL could not be induced in any animal in group 3 (p = 0.01).
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Atrial Activation Sequence During Sinus Rhythm
Atrial activation sequence maps in group 1, during sinus rhythm, demonstrated a line of conduction block corresponding to the site of the suture line along the CT (Fig 2). As the wavefront emanated from the region of the sinus node, it encountered a zone of conduction block along the lateral portion of the Fontan suture line on the right atrial free wall. The impulse broke across the suture line at its inferior-most aspect and propagated up the free wall of the atrium. The impulse reached the septal surface by traveling around either side of the inferior vena cava and continued uniformly and rapidly along the septum in a caudocranial direction. The septal portion of the lateral tunnel suture line and the atriotomy did not significantly alter conduction. In group 4, when the pericaval and septal portions of the suture line were eliminated, there were no significant differences in conduction during sinus rhythm (Fig 3).
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). Breakthrough again occurred at the caudal aspect of the suture line, allowing the wavefront to travel up the free wall. However, time isochrones along the CT manifest less ``crowding,'' suggesting more rapid conduction of the propagating impulse compared with groups 1 and 4. In group 3, conduction block was no longer evident along the free wall (Fig 5). The wavefront traveled unimpeded along the septal and free wall surfaces. As in group 2, isochronous lines along the free wall proximal to the site of the CT are less crowded than in groups 1 and 4.
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). Mean conduction velocity along the CT, normally 0.9 to 1.2 m/s [18, 19], was unaffected during sinus rhythm in group 2 (1.04 ± 0.17 m/s) and group 3 (1.01 ± 0.12 m/s). Conduction velocity was significantly reduced (p < 0.01) in those groups in which the CT was included in the suture line. Longitudinal conduction velocity along the CT was 0.63 ± 0.10 m/s in group 1 and 0.44 ± 0.13 m/s in group 4.
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). The wavefront traveled up the free wall, around the superior vena cava, and onto the septal surface, unabated by the septal portion of the suture line. The impulse then coursed inferior to the inferior vena cava and back onto the free wall to complete the reentrant circuit. Both clockwise and counterclockwise rotation patterns were observed. Atrial activation during reentry in group 4 did not differ significantly from that in group 1 (Fig 7). In group 2, conduction block on the free wall similarly created a corridor bounded inferiorly by the tricuspid annulus, which was integral to sustaining reentry (Fig 8). As observed during sinus rhythm in this group, the wavefront moved relatively rapidly along the site corresponding to the CT; the resultant AFL cycle length was significantly shorter than in groups 1 and 4.
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Conduction Block Imposed by the Free Wall Segment of the Lateral Tunnel Suture Line
Conduction block along the lateral portion of the Fontan suture line on the right atrial free wall established a protected isthmus between it and the tricuspid annulus, which was critical for reentry (see Fig 6
). Incorporation of the free wall segment of the suture line into the atriotomy (group 3) eliminated this block during sinus rhythm and was presumably the reason AFL could not be induced in this group of dogs. The 1 dog in group 2 that did not exhibit block during sinus rhythm also did not have inducible AFL.
Slow Longitudinal Conduction Along the Crista Terminalis
In the absence of an excessively long pathway over which a reentrant wavefront propagates, slowing of the wave in some part of its circuit must occur so that sufficient time elapses for the tissue to be reentered to recover excitability [22]. In addition to altering transverse conduction, placement of a suture line along the CT significantly attenuated conduction in the rostrocaudal direction. When both conduction block along the free wall segment of the lateral tunnel suture line and slow longitudinal conduction along the CT were present (groups 1 and 4), the propensity of AFL to develop in the atria using programmed stimulation was increased.
In those cases in which the suture line was placed medial to the CT (group 2), preservation of rapid longitudinal conduction along the CT inhibited the inducibility of AFL despite the presence of conduction block along the free wall. Large doses of isoproterenol, presumably by shortening the refractory period of myocytes, were required in these dogs to facilitate the initiation of AFL. Furthermore, the AFL cycle lengths were significantly shorter in this group. That these shorter cycle lengths were the result of preserved rapid conduction along the CT and not a consequence of isoproterenol is supported by the relatively long cycle lengths of AFL obtained in those 2 cases in group 1 in which AFL was induced after isoproterenol was administered.
Anisotropic conduction is a well-recognized characteristic of the CT. Normal conduction velocity along the longitudinal axis of the CT is extremely rapid, ranging from 0.9 to 1.2 m/s [18, 19]; conduction in the transverse direction is approximately 0.6 m/s. Muscle fiber orientation and gap junction arrangements are major factors contributing to this phenomenon [23]. Suture injury to the CT minimizes anisotropic conduction. Anatomic discontinuity around the CT hinders rapid preferential longitudinal conduction, which is usually inhibitory in cycles of evoked repetitive activity when the wavefront arrives prematurely at its site of origin and is blocked. Suppression of rapid longitudinal propagation effectively prolongs intraatrial conduction time. This increases the window of vulnerability to reentry since the recovery period of myocytes between beats is longer. This may have clinical relevance; intraatrial conduction has been demonstrated to be prolonged in patients with AFL after the Fontan operation [24, 25].
The Role of the Crista Terminalis in Atrial Flutter
The importance of the CT with respect to the initiation and maintenance of circus movement intraatrial reentry has been established in numerous animal models. Naturally occurring discontinuity between the upper and lower portions of the CT [13], suture ligation of the CT [13], and crush lesions placed within the CT [14, 15] have all been associated with AFL. Electrophysiologic findings have also been correlated with anatomic factors [26–28]. After epicardial ligation of the CT, prolongation of intraatrial conduction time from the high to low right atrium was demonstrated, as in the present study. Slow conduction during AFL was observed around the CT or a thick pectinate muscle branching from it. Even in models in which clearly defined anatomic barriers are not present, the CT appears critical for reentry. In both the sterile pericarditis [29] and right atrial enlargement models of canine AFL [30], long arcs of functional conduction block between the caval orifices, corresponding to the site of the CT, have been identified.
The results of our study may also offer insight into the underlying mechanisms of spontaneous human AFL. The CT has been demonstrated to be a barrier to conduction in the common form of naturally occurring human AFL [31, 32]. Anisotropic conduction in the vicinity of the CT creates a functional barrier between the posterior and lateral walls of the right atrium which, when added to the orifices of the cavae, constitutes a large enough central obstacle to potentially sustain reentrant activation. It is intriguing to postulate that perhaps microscopic structural abnormalities in the CT precipitate circus movement macroreentry. Although limited pathologic studies to directly implicate histologic irregularities of the CT in the pathogenesis of AFL have been reported, tangential references to sclerotic patches and diffuse fibrotic changes in the region of the CT exist [33]. A case report of a giant right atrial aneurysm that presented with AFL is interesting in that its location was along the right atrial free wall, extending from the superior to the inferior vena cava, and its excision terminated the arrhythmia [34].
Clinical Implications
Atrial flutter after the Fontan operation is a significant cause of morbidity and mortality for many children. Uncontrolled AFL may precipitate cardiac failure, hemodynamic deterioration, and sudden death [2, 6]. As the indications for the Fontan procedure expand to more complex congenital heart malformations, growing numbers of patients will emerge who are vulnerable to the hazards of postoperative supraventricular arrhythmias. The management of AFL after the Fontan procedure is very problematic. The underlying congenital lesions and the surgical procedures that create the substrate for the development of these arrhythmias are often associated with a marginal hemodynamic status, limiting the options for medical arrhythmia management. Antiarrhythmic drugs may aggravate sinus node dysfunction or cause deterioration of ventricular function [6]. In addition, the presence of a baffle severely inhibits transvenous catheter ablation of AFL after the modified Fontan operation.
A modification of the Fontan operation has been described in which a patch was employed to septate the right atrium. The patch attachments avoided the CT. No postoperative arrhythmias were observed, although follow-up was relatively short [35]. The results of our study suggest that a modification of the lateral tunnel suture line that incorporates the free wall portion of the suture line into the atriotomy, which is made anterior and parallel to the CT, may substantially reduce the incidence of postoperative AFL. Anecdotally, some centers are currently using such an approach; a multicenter comparison may be of interest.
Limitations of the Study
The animal model employed in this study had normal cardiac anatomy. The anatomic and physiologic influences of complex congenital cardiac malformations were not present. Atrial flutter was artificially induced by burst pacing and premature extrastimulation. Atrial flutter was also induced on cardiopulmonary bypass after the insertion of mapping electrodes, thus eliminating any effect of atrial or ventricular filling on the induction or maintenance of AFL. These induced arrhythmias may not accurately represent spontaneous AFL after the Fontan operation.
As this was an acute study design, none of the alterations in atrial structure, such as hypertrophy and fibrosis, present chronically in patients who have undergone the Fontan operation were present. These histologic changes may also contribute to abnormalities in atrial conduction.
Conclusions
In an acute canine model of the modified Fontan operation, conduction block imposed by the lateral tunnel suture line is an essential component of the AFL circuit. The inducibility of AFL is increased by suture line placement along the CT. Slow conduction, resulting from injury to the CT, promotes this increased inducibility. Avoidance of the CT may reduce the incidence of AFL in children undergoing the modified Fontan operation.
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Acknowledgments |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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This work was supported by National Institutes of Health grants HL 32257 and HL 33722.
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Footnotes |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Address reprint requests to Dr Huddleston, Department of Surgery, St. Louis Children's Hospital, One Children's Pl, Suite 5W24, St. Louis, MO 63110.
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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