Abstract
Background
Twin atrioventricular nodes (AVNs) occasionally occur in congenitally corrected transposition of the great arteries (ccTGA).
Case Summary
A 14-year-old adolescent girl with ccTGA died suddenly after cardiopulmonary arrest. The electrocardiogram showed QRS widening from age 6. At autopsy, a Rastelli conduit and a fibrotic scar from ventricular septal defect patch closure were present. Serial sections revealed isolated anterior and posterior AVNs. The posterior AVN continued into an elongated His bundle that was disrupted by fibrosis, whereas the anterior AVN was interrupted by fibrofatty tissue.
Discussion
QRS widening was likely caused by interruption of the elongated His bundle. Although posterior-dominant AVN is uncommon, it should be considered when planning surgery for ccTGA.
Take-Home Message
A posterior-dominant AVN is uncommon; however, it should be considered when planning surgery for ccTGA with usual atrial arrangement.
Key Words: AV conduction system, conduction disturbance, His bundle, pathology, twin AV node, ventricular septal defect
Visual Summary
Congenitally corrected transposition of the great arteries (ccTGA) is a congenital heart disease characterized by discordant atrioventricular (AV) and discordant ventriculoarterial connections. In the absence of associated cardiac malformations, patients may remain asymptomatic, although some develop progressive heart block later in life.1 Commonly, there are associated cardiac defects, such as ventricular septal defects (VSD) and pulmonary stenosis (PS),2 that require surgical repair involving patch closures of VSDs together with the Rastelli procedure, which uses an extracardiac artificial conduit for correcting PS.3
In ccTGA with situs solitus, the AV conduction system is usually sited anteriorly and connected to an anterior AV node located in the right atrium in the vicinity of mitral-pulmonary valvar fibrous continuity, where the His bundle penetrates through to descend as the AV conduction bundle along the anterocephalad part of the ventricular septum or along that margin of a coexisting VSD. The AV conduction bundle is usually long and branches into the left bundle branch that descends along the endocardium on the right aspect of the septum whereas the right bundle branch passes to the left side of the septum corresponding to the right-sided morphological left ventricle and left-sided morphological right ventricle, respectively. A normally located posterior AV node located in the triangle of Koch is usually hypoplastic. In a few cases, there may be 2 AV nodes, whereby one is located anteriorly and another is located posteriorly, each continuing into an AV conduction bundle.4 Rarely, the presence of 2 nodes, each giving rise to an AV conduction bundle that connects to form a conduction bundle sling, may be related to better alignment of atrial and ventricular septa in hearts with stenosis or atresia of the pulmonary outflow tract.5 Recognizing abnormalities in the location of the AV conduction system is an important factor when planning a safe surgical intervention for ccTGA.
History of Presentation
A 14-year-old adolescent girl with surgically repaired ccTGA experienced cardiopulmonary arrest. Cardiopulmonary resuscitation was attempted; however, the patient died. No external injuries or toxicological abnormalities were identified. Despite a whole-body computed tomography examination, no suspected cause of death was identified in the internal organs, and a forensic autopsy was performed.
Past Medical History
At 2 years of age, she had undergone a Rastelli procedure involving reconstruction of the connection between the morphological left ventricle and the pulmonary artery using an artificial conduit, as well as patch closures of atrial and ventricular septal defects. Starting at 6 years of age, electrocardiograms (ECGs) had shown a widened QRS pattern and complete right bundle branch block (Figure 1), as well as occasional premature ventricular contractions. However, she had no conspicuous symptoms and was not taking medications.
Figure 1.
Changes in the Patient's QRS Morphology on the 12-Lead Electrocardiogram
After the Rastelli procedure, the width of the QRS complex increased without severe changes in the electrical axis. This change was less pronounced and more persistent.
Investigations (Autopsy Findings)
Macroscopic findings
The heart weighed 372 g. The AV and aortic valve annuli were not significantly dilated. The artificial conduit from the Rastelli procedure was found at a site corresponding to the right-sided ventricular outflow. A scar from a patch closure was clearly observed from the perspective of the morphological right ventricle as a recess caused by the VSD (Figure 2). There were no significant abnormal findings (eg, deformities or inflammatory changes) around the sites of previous procedures. On short-axis sections of both ventricles, an old fibrotic scar with no recent myocardial necrosis was noted in the lateral wall of the morphological left ventricle (ie, the right-sided morphological left ventricle that was connected to the pulmonary artery conduit). This ischemic fibrotic lesion was thought to be a potential substrate for a lethal ventricular arrhythmia.
Figure 2.
Macroscopic Photograph of the Septal Atrioventricular Junction
(A) Macroscopic endocardial view of the right side of the heart. The RA is connected to the morphological LV through the MV. An artificial conduit has been used to repair the outflow tract. A VSD patch is noted behind the mitral valve leaflets. The anterior node is larger than the posterior node. The anterior node is contiguous with the His bundle but is disrupted at the His transition site. The smaller posterior node is contiguous with the His bundle. It moves around the lower limb of the VSD patch and has an intermittent appearance. The red dot outlined in yellow indicates the smaller His bundle, and the blue dot indicates the larger anterior node. The red cross indicates the site of disruption of the His bundle extending from the posterior node. The yellow lines indicate the distribution of the His and bundle branches. The blue dotted line indicates disruption of the His bundle connection. The black square indicates the area removed for serial sections. Bar = 10 mm. (B) Macroscopic endocardial view of the left side of the heart. The closed VSD is located in a hole-like lesion. The estimated location of the posterior node (blue dot) is indicated through the RBB (blue line). Ao = aorta; CS = coronary sinus; LV = left ventricle; MV = mitral valve; RA = right atrium; RBB = right bundle branch; RV = right ventricle; SVC = superior vena cava; TV = tricuspid valve; VSD = ventricular septal defect.
Microscopic exploration of the atrioventricular conduction system
The AV conduction system was histologically assessed to reveal changes conducive to the widened QRS morphology noted on prior ECGs. After fixation in formalin, a part of the AV septal junction, including the AV conduction system (from the AV node to the right bundle branch), was removed (Figure 2) and embedded in paraffin. Serial sections with a thickness of 7 μm were prepared at 70-μm intervals. The sections were stained with hematoxylin and eosin and Masson trichrome.
Microscopic findings
The AV nodes were located at 2 distinct isolated sites identified as a posterior node and an anterior node (Figure 3). The posterior node was located beside the coronary sinus opening at a position similar to the usual location within the triangle of Koch in a structurally normal heart. The nodal length was 3.2 cm, and the nodal tissue was adjacent to the central fibrous body where the conduction tissues penetrated to continue as the His bundle. The His bundle penetrating the fibrous body was 1.8 mm in length, and the subsequent non-branching portion was prolonged to 5.4 mm. Beyond this site, the bifurcation portion leading to the left bundle branch was located close to the fibrous scar caused by the patch closure for the VSD. Along this scar, the bundle running beneath the endocardium showed atrophic changes and was indistinct in several portions (Figure 4); however, beyond the origin of the right bundle branch, it was preserved and ran toward the left ventricular endocardium.
Figure 3.
Histological Analysis of the Atrioventricular Junction on Serial Sections (Masson Trichrome Stain)
(A) The posterior AVN is located on the central fibrous body. The offset of the attachment to the TV and MV is small and shows a horizontal plane shape. (B) The invagination of the transition from the AVN to the His bundle goes straight down into the central fibrous body. (C) The His bundle penetrates the central fibrous body and continues to the summit of the VS. (D) The His bundle elongates and passes along the edge of the VSD, and the ant AVN is located above the rim of the VSD patch in this section. (E) This component of the His bundle is atrophic and indistinct (yellow arrow). A component of the ant AVN invaginates into the fibrous tissue (cardiac fibrous skeleton). (F) The His bundle is contiguous with a component of the RBB. A component of the ant AVN is disrupted at this section. Bars = 5 mm. Yellow dotted areas indicate AVN and the His bundle. Ant = anterior; AVN = atrioventricular node; VS = ventricular septum; other abbreviations as in Figure 2.
Figure 4.
Interrupted Site of the His Bundle (Masson Trichrome Stain)
The conduction cells are unclear at the site around the fibrous scar tissue after the VSD patch closure (yellow arrow). Bar = 2.5 mm. Abbreviations as in Figure 3.
The anterior node showed a completely isolated location in the right atrium on the anterior margin of the mitral valve annulus (of the right-sided morphological left ventricle), and the distance from the posterior node was approximately 4.5 cm. The nodal tissue was 4.2 mm in longitudinal length and continued into the His bundle, passing into the fibrous tissue of mitral-pulmonary valvar continuity. However, it was completely disrupted and replaced with fibrofatty tissue. The QRS complex was widened on ECGs after the Rastelli procedure, and an intraventricular conduction disturbance was considered a likely cause for this alternation. The morphological changes in the extended AV conduction system at the nonbranching portion of the His bundle and the fibrous changes caused after the operation were considered to be potential reasons for the abnormal ECG findings.
Discussion
In this case, 12 years had passed since the surgical repair, which is a common time period for ventricular arrhythmias to occur,6,7 and a relatively large chronic fibrous scar compatible with an arrhythmic substrate was found on transverse sections of both ventricles. Life expectancy in these patients is reduced, and only 50% of patients with associated lesions, such as VSDs or PS, will survive to 40 years of age, with patients generally dying of congestive heart failure or dying suddenly, presumably of ventricular arrhythmia.8 However, the ECG changes found in her QRS duration were not necessarily related to ventricular arrhythmias; therefore, a detailed evaluation by serial sectioning of the AV conduction system was performed.
Two AV nodes, or so-called twin AV nodes, were detected during this analysis.4 This abnormal morphology of the AV conduction system can cause conduction disturbances throughout a patient's lifetime, and fibrotic changes in the bundle branches have also been reported to be a source of conduction disturbances.4 In the present case, the major and functional anterior AV node was connected to components of the disrupted His bundle. The posterior node; however, showed a hypoplastic size. On serial sections, continuity with the His bundle was observed, as in hearts without structural abnormalities; however, the invagination angle into the central fibrous body as it made the shift to the His bundle was unusual and extended straight down beneath the AV node. The dominant location pattern of the posterior AV node was also rare,9 as was the extended His bundle running along the inferior edge of the VSD.
Furthermore, the heart exhibited a deep hole related to the VSD. The patch had been placed on the right side of the defect, and the offsets of the mitral and tricuspid valve attachments were small (nearly at the same level, showing a horizontal shape of the central fibrous body). These characteristics of the AV junction suggest a straddling mitral valve, indicating posterior node dominance and a connection to the His bundle.9 The surgical procedure for VSD patch closure was possibly performed under the assumption that the His bundle was running along the upper edge of the VSD, which may be the cause for the close location of the patch suture to the His bundle and may also have induced the ventricular conduction disturbances that led to a widening of the QRS complex on the ECG. Another possibility is that it was caused by the sling formation along the edge of the VSD.10 In this case, both the anterior and posterior components of the AV node may have formed a sling arc contiguous with the His bundle. However, this was uncertain because of the mature fibrotic scar around the VSD patch.
Conclusions
In this case, we confirmed that the His bundle extended from the posterior AV node, which is rare in ccTGA hearts. Impairments in the conduction system caused by the surgical procedure may have been related to the initiation of or vulnerability to a lethal ventricular arrhythmia, and this is an important variation to keep in mind when devising a safe surgical strategy for repair of ccTGA hearts.
Visual Summary.
A Posterior-Dominant AVN Is Uncommon in Patients With ccTGA
Impairments in the conduction system extending from the posterior AVN caused by the surgical procedure have been related to the changes in QRS morphology on the electrocardiogram and may also have increased the patient's vulnerability to lethal ventricular arrhythmias. The red cross and the blue arrow indicate the site where the His bundle is atrophic and indistinct. Yellow circles with blue and red dot indicate the anterior and posterior AVNs, respectively. Ant = anterior; ASD = atrial septal defect; AVN = atrioventricular node; BT = Blalock-Taussig shunt; ccTGA = corrected transposition of the great arteries; CS = coronary sinus; lt. = left; L-TGA = levo-TGA; MV = mitral valve; PA = pulmonary artery; RA = right atrium; RBBB = right bundle branch block; rt. = right; SVC = superior vena cava; TV = tricuspid valve; VS = ventricular septum; VSD = ventricular septal defect.
Funding Support and Author Disclosures
The authors have reported that they have no relationships relevant to the contents of this paper to disclose.
Take-Home Messages
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•
A posterior-dominant atrioventricular node is uncommon; however, it should be kept in mind when devising a safe surgical strategy for corrected transposition of the great arteries that has usual atrial arrangement.
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Impairments in the conduction system caused by the surgical procedure have been related to changes in QRS morphology on the electrocardiogram and may have been associated with the initiation of or vulnerability to a lethal ventricular arrhythmia.
Acknowledgment
The authors sincerely thank Masahiro Misawa for kindly providing the previous clinical data on this case.
Footnotes
The authors attest they are in compliance with human studies committees and animal welfare regulations of the authors’ institutions and Food and Drug Administration guidelines, including patient consent where appropriate. For more information, visit the Author Center.
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