Ann Thorac Surg 1995;59:352-360
© 1995 The Society of Thoracic Surgeons
Anatomic Spectrum of Abnormal Ventriculoarterial Connections: Surgical Implications
Athos Capuani, MD,
Hideki Uemura, MD,
Siew Yen Ho, PhD,
Robert H. Anderson, MD
Department of Paediatrics, National Heart and Lung Institute, London, United Kingdom
Accepted for publication September 15, 1994.
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Abstract
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To clarify the salient anatomic features of surgical significance, we investigated 33 specimens representing the spectrum of abnormal ventriculoarterial connections. In those with tetralogy of Fallot or double-outlet right ventricle with subaortic ventricular septal defect, the muscular outlet septum separating the subarterial outflow tracts was always inserted into (or in front of) the anterior limb of the septomarginal trabeculation (septal band). In those having double-outlet right ventricle with doubly committed ventricular septal defect, the outlet septum was lacking. When the ventricular septal defect was in subpulmonary position, with either double-outlet or discordant ventriculoarterial connections, the outlet septum was attached to the posterior limb of the septomarginal trabeculation. The outlet septum was deviated into the subpulmonary outlet in hearts with discordant ventriculoarterial connections and pulmonary stenosis. It is the interrelations between the septomarginal trabeculation, the outlet septum, and the ventriculoinfundibular fold that hold the key to the understanding of surgical anatomy and determine the optimal choice of procedure for definitive biventricular repair.
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Introduction
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T here is a spectrum of cardiac malformations that reflect an abnormal transfer during development of the aorta from the right to the left ventricle. Often known as ``conotruncal'' anomalies, a key feature of the morphology is the location and insertion of the outlet (or infundibular) septum relative to the remainder of the muscular ventricular septum [1]. The extent of the inner curvature of the heart separating the attachments of atrioventricular and arterial valves is also important, as is the degree of formation of the posterior limb of the septomarginal trabeculation (septal band) [2]. From the surgical stance, within this range of pathology, some hearts can be corrected so as to achieve a biventricular repair simply by closing the ventricular septal defect so that the aorta is re-routed to the left ventricle. In others, an intracavitary tunnel must be created within the right ventricle to achieve this effect [3–6]. Still other hearts can be corrected by re-routing the ventricular septal defect so that it opens from the left ventricle into the pulmonary trunk, a maneuver that then necessitates additional switching at either the arterial or atrial levels to correct the circulations [7]. In hearts with pulmonary or subpulmonary stenosis, however, the latter procedure cannot be accomplished without concomitant relief of the initial area of stenosis. Therefore, the hearts with such accompanying obstructive lesions in the subpulmonary area are those in which either the Rastelli [8], the Nikaidoh [9], or the REV [10, 11] procedures can be used.
To understand the optimal applications of these varied surgical procedures, it is crucial to understand the anatomic interrelations of the various components of the ventricular outflow tracts [1, 2]. In this respect, it should be noted that a recent report [6] discussed in detail the location of the ventricular septal defect in double-outlet right ventricle, yet paid much less attention to the interrelationships of the components of the outflow tracts and the anatomic borders of the ventricular septal defect. Therefore, in this investigation we sought to establish these relationships by examination of an autopsied series of hearts that demonstrated the range of so-called conotruncal malformations.
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Material and Methods
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We examined selected hearts from the cardiopathologic collection of the Royal Brompton Hospital, all with usual atrial arrangement and concordant atrioventricular connections, having either Fallot's tetralogy (5 patients), double-outlet right ventricle (23 patients), or complete transposition with ventricular septal defect (5 patients).
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Results
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Tetralogy of Fallot
Tetralogy of Fallot exemplifies the divorce of those muscular components that, in the normal heart, form the supraventricular crest (Fig 1
). Thus, the outlet septum in tetralogy is seen as an independent muscular structure, but one that separates the outflow tracts one from the other rather than contributing to the muscular septum between the cavities of right and left ventricles as in the normal heart. Indeed, the essence of tetralogy of Fallot is that the outlet septum is exclusively a right ventricular structure (Fig 2). In some hearts, however, depending on the extent of the subpulmonary infundibulum, there can be a sleeve of freestanding infundibular musculature at the distal end of the subpulmonary outlet, with offsetting of the leaflets of the aortic and pulmonary valves. In other specimens, in contrast, the leaflets of the aortic and pulmonary valves are at the same level on opposite sides of the outlet septum. Irrespective of this, the outlet septum merges with the anterior limb of the septomarginal trabeculation. The degree of overriding of the aorta then depends on the extent of rightward displacement of the outlet septum and the degree of formation of the ventriculoinfundibular fold. In most specimens, the ventriculoinfundibular fold becomes attenuated at the posteroinferior margin of the ventricular septal defect so that there is fibrous continuity between the leaflets of the aortic and tricuspid valves (see Fig 2). We use this feature to categorize the septal defect as being perimembranous. In the minority of cases, the posterior limb of the septomarginal trabeculation fuses with the ventriculoinfundibular fold, producing muscular discontinuity between the leaflets of the aortic and tricuspid valves. When viewed from the right ventricle, therefore, the locus for placement of the patch to ``close'' the defect is exclusively muscular.
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Fig 1. . These dissections of a normal heart show the relationships of the septomarginal trabeculation (SMT) (septal band) and the supraventricular crest. (a) Dissection in which the roof of the right ventricle has been removed. It shows that the greatest part of the supraventricular crest is the inner curvature of the parietal wall of the right ventricle (the ventriculoinfundibular fold [Vent. inf. fold]). (Pulm. valve = pulmonary valve.) Further dissection (b) reveals that part of this fold forms the freestanding subpulmonary infundibulum (Sub-pulm. infundibulum). There is no ``outlet septum'' as such identified in the normal heart. Note also the location of the triangle of Koch, seen well in a. (Ant. limb = anterior limb.)
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Fig 2. . In tetralogy of Fallot, the components of the supraventricular crest of the normal heart have sprung apart. The ventricular septal defect, overridden by the aortic valve, is between the limbs (A,P) of the septomarginal trabeculation (heavy stipple). The outlet septum (fine stipple) is a right ventricular structure, attached septally to the anterior limb of the trabeculation. The ventriculoinfundibular fold (wavy lines) separates the leaflets of the aortic and tricuspid valves, but stops short of the posterior limb so that there is valvar continuity posteroinferiorly. The convention of shading is used in similar fashion through all the subsequent illustrations. (Pulm. trunk = pulmonary trunk.)
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Double-Outlet Right Ventricle
WITH SUBAORTIC VENTRICULAR SEPTAL DEFECT.
It is our practice to define hearts as showing double-outlet right ventricle when more than half of the leaflets of both arterial valves are supported by right ventricular structures. When defined in this fashion, the hearts can show the ventriculoarterial connection of double outlet together with the infundibular morphology of tetralogy of Fallot. Such hearts were found within the collection (Fig 3). These hearts, with a subaortic ventricular septal defect, are to be distinguished from classic double-outlet right ventricle with subaortic ventricular septal defect and subaortic and subpulmonary infundibular structures (Fig 4). In most hearts with such ``classic'' double outlet, the aortic valvar leaflets are exclusively connected within the right ventricle. Even in these hearts, there is marked variability in the extent of the ventriculoinfundibular fold. If the fold is well represented, there is a complete muscular infundibulum supporting the aortic leaflets and separating these from the leaflets of the mitral and tricuspid valves (see Fig 4). If the fold is less well formed posteriorly, there may be aortomitral continuity, whereas anteriorly the leaflets of the aortic valve are separated from those of the tricuspid valve. If the fold is also attenuated anteriorly, there is aortotricuspid continuity in addition to aortomitral and mitral–tricuspid continuity. In these hearts with subaortic ventricular septal defect, the outlet septum is usually a well-formed muscular structure that inserts in front of or with the anterior limb of the septomarginal trabeculation. This produces a complete subpulmonary infundibulum that, as in tetralogy, can be a freestanding sleeve of infundibular musculature, as can the distal component of a muscular subaortic infundibulum.
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Fig 3. . In this heart with tetralogy of Fallot, the outlet septum is grossly hypoplastic and the leaflets of the aortic valve are tethered exclusively within the right ventricle. There is double-outlet ventriculoarterial connection, but with fibrous continuity between the leaflets of the tricuspid, aortic and mitral valves. (Pulm. trunk = pulmonary trunk.)
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Fig 4. . In this example of classic double-outlet right ventricle, the ventricular septal defect, between the limbs of the septomarginal trabeculation ( P,A) is directed to the aortic valve owing to the location of the outlet septum. (Pulm. valve = pulmonary valve.)
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WITH DOUBLY COMMITTED VENTRICULAR SEPTAL DEFECT.
The key to hearts with double-outlet right ventricle and doubly committed septal defect (Fig 5) is complete absence not only of the muscular outlet septum but also of the adjacent components of infundibular musculature that, in the classic variant, support the adjacent (``facing'') leaflets of the aortic and pulmonary valvesfig 5. The extent of the ventriculoinfundibular fold continues to determine the presence or absence of continuity between the leaflets of the arterial and atrioventricular valves, whereas the relationship between the posterior limb of the septomarginal trabeculation and the ventriculoinfundibular fold determines whether the defect is perimembranous or has a muscular posteroinferior rim.
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Fig 5. . In this heart with double-outlet ventriculoarterial connection and doubly committed ventricular septal defect, absence of the outlet septum together with absence of the septal components of both infundibulums permit the orifices of both arterial trunks to ride the crest of the ventricular septum. Fusion of the posterior limb of the septomarginal trabeculation (P) with the ventriculoinfundibular fold forms a muscle bar separating the leaflets of the aortic and tricuspid valves. (Pulm. valve = pulmonary valve.)
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HEARTS WITH SUBPULMONARY VENTRICULAR SEPTAL DEFECTS.
When the outlet septum is present but merges posteriorly with either the ventriculoinfundibular fold (separating the leaflets of the aortic and tricuspid valves) or with the posterior limb of the septomarginal trabeculation (or both), then the septal defect is subpulmonary. This arrangement usually produces a complete subaortic infundibulum anteriorly within the right ventricle (Fig 6), the distal portion of which can again be a freestanding sleeve of infundibular musculature. Alternatively, the ventriculoinfundibular fold can be attenuated to permit continuity between the aortic and tricuspid valvar leaflets (Fig 7). With this arrangement, when the pulmonary valve is positioned exclusively above the right ventricle, the ventriculoarterial connection is that of double-outlet right ventricle (see Figs 6, 7). The presence or absence of fibrous continuity between the leaflets of the pulmonary and mitral valves depends on the prominence of the ventriculoinfundibular fold. A spectrum of malformation is seen in which the leaflets of the pulmonary valve come to be attached within the left ventricle (Figs 8, 9). Within our definitions, when more than half of the circumference of the pulmonary valve is supported by the left ventricular structures, the ventriculoarterial connections are diagnosed as discordant rather than double outlet (see Fig 9). The overall spectrum of hearts with subpulmonary ventricular septal defect, nonetheless, can be considered to represent the Taussig-Bing malformation. Throughout this malformation, if the posterior limb of the septomarginal trabeculation fuses with the ventriculoinfundibular fold, there will be a muscular posteroinferior rim to the defect (see Fig 7). If there is discontinuity between these structures, the leaflets of the mitral and tricuspid valves will be in fibrous continuity in the posteroinferior rim and the defect will be perimembranous (see Fig 6).
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Fig 6. . In this heart, an example of the Taussig-Bing malformation, the ventricular septal defect opens in subpulmonary position because the outlet septum is fused with the ventriculoinfundibular fold rather than with either limb of the septomarginal trabeculation. There is fibrous continuity between the leaflets of the tricuspid and mitral valves (perimembranous defect). (Pulm. valve = pulmonary valve.)
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Fig 7. . In this example of a Taussig-Bing heart (compare with Fig 6 ), the outlet septum fuses with both the ventriculoinfundibular fold and the posterior limb of the septomarginal trabeculation so that the ventricular septal defect has a muscular posteroinferior rim. Because of attenuation of the ventriculoinfundibular fold, there is fibrous continuity between the leaflets of the aortic and tricuspid valves. (Pulm. trunk = pulmonary trunk.)
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Fig 8. . In this example of the Taussig-Bing malformation, with a muscular posteroinferior rim to the subpulmonary ventricular septal defect, the pulmonary valve overrides the crest of the ventricular septum such that its greater part is attached within the left ventricle (see Fig 9) (Pulm. trunk = pulmonary trunk.)
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Fig 9. . As shown in this view of the left ventricle of the heart shown in Figure 8, the pulmonary valve (Pulm. valve) originates mostly from the left ventricle. The ventriculoarterial connections in this case, therefore, are discordant (complete transposition).
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A significant variation in this sequence was seen in one of our hearts. In this specimen, the outlet septum was at right angles with the remainder of the muscular ventricular septum, and the ventricular septal defect, beneath the anterior limb of the septomarginal trabeculation, was in the subpulmonary position (Fig 10). The outlet septum merged posteriorly with the ventriculoinfundibular fold and the posterior limb of the septomarginal trabeculation. Inferiorly, however, the outlet septum was continued as an apical shelf of muscle that divided completely the apical component of the right ventricle (double-chambered right ventricle). This arrangement seemed to sequestrate the most anterior and leftward portion of the right ventricle as part of the left ventricle (see Fig 10). A small, slitlike, ventricular septal defect with exclusively muscular rims also was present in the subaortic position.
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Fig 10. . In this case, the outlet septum is inserted across the doubly committed ventricular septal defect, dividing it into subaortic (VSD1) and subpulmonary (VSD2) components. An apical continuation of the outlet septum forms a muscular shelf that sequestrates the subpulmonary component of the morphologically right ventricle from the rest of the chamber, giving the spurious impression of complete transposition. In reality, the heart shows an extreme form of both double-outlet and double-chambered right ventricle. (Pulm. trunk = pulmonary trunk.)
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Posterior Deviation of the Outlet Septum
The outlet septum can be deviated posteriorly to be inserted within the left ventricular outflow tract. With this arrangement, when seen from the right ventricle, the defect is subaortic. Indeed, the leaflets of the aortic valve are attached in part within the left ventricle. The deviated position of the outlet septum produces subpulmonary obstruction. As with the other hearts, depending on whether the ventriculoinfundibular fold fuses or does not fuse with the posterior limb of the septomarginal trabeculation, the ventricular septal defect can be perimembranous or can have a muscular posteroinferior rim.
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Comment
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The association between hearts having tetralogy of Fallot, double outlet from the morphologically right ventricle, and complete transposition (concordant atrioventricular with discordant ventricular arterial connections) has long fascinated anatomists and embryologists [12, 13]. With advances in surgical techniques, the interest in these lesions has achieved more practical importance. Differences in description and categorization that previously were of academic interest can now potentially color the procedure chosen for surgical correction. Many such options are available, including simple patching of the ventricular septal defect into the aorta, more complex intraventricular re-routing procedures involving various shaped patches, sometimes with tubular conduits, and those requiring connection of the ventricular septal defect to the pulmonary trunk. The latter procedure, of necessity, involves also an additional ``switching'' of the circulations at either atrial or great arterial levels. These techniques for switching offer additional options, such as Senning or Mustard procedures at atrial level, or coronary arterial relocation versus the Damus-Stansel-Kaye procedure at the level of the arterial trunks. The introduction of still further surgical options, such as the Nikaidoh [9] and the REV [10, 11, 14] procedures, has reemphasized the need for the surgeon to appreciate the nature of the various muscular components of the outflow tracts, particularly the potential for their resection and relocation.
The distinction between the three components of the outflow tracts as outlet septum, ventriculoinfundibular fold, and septomarginal trabeculation was made as long ago as 1977 [2]. The results of our present study, conducted from a surgical stance, confirm the advantages of analyzing the muscular components of the outflow tracts in this proposed fashion. It has, nonetheless, proved necessary to modify the initial concept in one important way. Initially, we had argued that in the normal heart, the musculature supporting those leaflets of the pulmonary valve that faced the aorta was composed of outlet septum. We now know that this is not the case. The distal component of the subpulmonary infundibulum of the normal heart is, in reality, a freestanding sleeve of right ventricular musculature. The outlet septum does not become recognizable as such until it is divorced from the ventriculoinfundibular fold, as in the lesions studied in this investigation. Because the components of the normal ``crista'' then achieve their own identity, it is preferable not to identify any single one as an abnormal supraventricular crest, but instead to describe each muscular structure in its own right.
The key feature then determining the sequence of malformations presently described is the relationship between the outlet septum and the remainder of the ventricular outlet musculature. When the outlet septum is attached and blends with (or is in front of) the anterior limb of the septomarginal trabeculation, then the ventricular septal defect, cradled in the limbs of the trabeculation, is positioned in the subaortic location (presuming the aorta to be the rightward and posterior of the two arterial trunks). This position of the outlet septum produces a discrete muscular subpulmonary infundibulum that varies in its extent depending on the length of the outlet septum and the size of the freestanding sleeve of subpulmonary musculature. A crucial step in the sequence of anomalies is seen with regression of the outlet septum in those hearts characterized by fibrous continuity between the leaflets of the aortic and pulmonary valves. An additional feature of these hearts is absence of the ``septal'' components of the subaortic and subpulmonary infundibula. When the outlet septum and adjacent infundibular components are lacking, the ventricular septal defect is doubly committed and both arterial valves are free to override the crest of the muscular ventricular septum. A further spectrum of malformation is seen extending toward double-outlet left ventricle. These are the hearts that Brandt and colleagues [15] suggested could be called double-outlet both ventricles.
The sequence of anomalies with double-outlet ventriculoarterial connection is continued in those hearts characterized by insertion of the outlet septum to the posterior limb of the septomarginal trabeculation. This attachment effectively directs the ventricular septal defect, still positioned between the limbs of the septomarginal trabeculation, into the pulmonary trunk (again presuming a rightward location of the aorta relative to the pulmonary trunk). This attachment of the outlet septum usually is associated with a complete muscular subaortic infundibulum located anteriorly within the right ventricle, but the arrangement can be modified by attenuation of the ventriculoinfundibular fold permitting aortic-to-tricuspid valvar continuity.
The location and insertion of the outlet septum is itself conditioned by other variables, particularly the extent of the ventriculoinfundibular fold and the interrelationship between fold and the posterior limb of the septomarginal trabeculation. It is the extent of the ventriculoinfundibular fold that determines whether or not the muscular infundibular structures are complete beneath both arterial valves. This feature is independent of the connection of the arterial valvar leaflets within the ventricular mass. Thus, both arterial valves can be exclusively connected within the morphologically right ventricle, and yet have their leaflets in fibrous continuity with those of the atrioventricular valves. A double infundibulum, therefore, is not an essential feature for both arterial valvar orifices to be exclusively connected within the right ventricle. Conventions that link together these features [16, 17] are, of necessity, artificial. Irrespective of such controversies, the vital surgical feature concerning the ventriculoinfundibular fold is that recognition of any structure interposed between the leaflets of the arterial and atrioventricular valves identifies it unequivocally as part of the inner heart curvature. Incisions through this fold take the surgeon outside the heart, and likely place at risk important branches of the major coronary arteries.
The relationship between the posterior limb of the septomarginal trabeculation and the ventriculoinfundibular fold determines the continuity or discontinuity between the leaflets of the mitral and tricuspid valves. When the structures fuse, the muscle bar thus formed protects the point of penetration of the axis of atrioventricular conduction tissue. When these structures do not fuse, there is mitral-to-tricuspid valvar continuity, often together with aortic continuity. The ventricular septal defect with this fibrous area as part of its border can then be categorized as being perimembranous [1]. The conduction axis is much more vulnerable when defects are perimembranous. In contrast, if a protecting muscle bar is present and substantial, it can be used safely for anchorage of sutures. If defects cradled between the limbs of the septomarginal trabeculation are restrictive and need to be enlarged surgically, it is the area related to the anterior limb that can be resected safely.
In drawing our conclusions regarding the described sequence of malformations, we have ignored several other crucial variables. Thus, we have examined only the series of hearts in which the aorta is basically rightwardly located relative to the pulmonary trunk. Very likely there is a further series of hearts in which the aorta is located leftward in relation to the pulmonary trunk. Furthermore and highly significant, variations are produced by the interrelationships of the arterial trunks themselves. These can be basically side-by-side, basically anteroposterior, or obliquely located [1, 18]. All of these independent variables must be taken into account when attempting to determine the most appropriate surgical procedures. Still further features, particularly the arrangement of the coronary arteries, will need to be considered if arterial operation is contemplated. Our investigation has shown, nonetheless, that it is the position of the outlet septum that determines the location of the ventricular septal defect relative to the subaortic and subpulmonary outflow tracts. This structure, and its differentiation from the ventriculoinfundibular fold, should be the major focus of diagnosticians and surgeons contemplating the optimal surgical treatment of so-called conotruncal malformations.
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Acknowledgments
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The work was supported by the British Heart Foundation and the Joseph Levy Foundation.
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Footnotes
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Address reprint requests to Dr Anderson, Department of Paediatrics, National Heart and Lung Institute, Dovehouse St, London SW3 6LY, UK.
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References
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Abstract
Introduction
