Ann Thorac Surg 2008;86:1321-1327. doi:10.1016/j.athoracsur.2008.06.050
© 2008 The Society of Thoracic Surgeons
Original Articles: Pediatric Cardiac
Morphologic Spectrum of Ventriculoarterial Connection in Hearts With Double Inlet Left Ventricle: Implications for Surgical Procedures
Hideki Uemura, MD, FRCSa,*,
Siew Yen Ho, PhDb,
Iki Adachi, MDb,
Toshikatsu Yagihara, MDc
a Department of Cardiothoracic Surgery, Royal Brompton Hospital, London, United Kingdom
b Cardiac Morphology Unit, Imperial College London and Royal Brompton Hospital, London, United Kingdom
c National Cardiovascular Center, Osaka, Japan
Accepted for publication June 9, 2008.
* Address correspondence to Dr Uemura, Department of Cardiothoracic surgery, Royal Brompton Hospital, Sydney St, London, SW3 6NP, United Kingdom (Email: h.uemura{at}rbht.nhs.uk).
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Abstract
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Background: This study was conducted to determine a morphologic spectrum of ventriculoarterial connection in double inlet left ventricle and implications for surgical procedures.
Methods: Examined were 54 autopsied heart specimens and 43 consecutive clinical patients.
Results: The hypoplastic and incomplete morphologic right ventricle was located leftward to the dominant ventricle in 62 and adjacent to the right atrium in 35. Common patterns were seen in 46 of 62 (74%) with the right ventricle leftward (discordant ventriculoarterial connection with the aorta left-anteriorly located ["SLL" type]) and in 28 of 35 (80%) with the right ventricle rightward (either the normally connected great arteries in 13 or discordant connections with the aorta right-anteriorly located in 15). In the remaining 23 hearts, the great arteries were unusually oriented in 7, the outlet septum was malaligned in 9, or the pulmonary trunk was atretic in 7. In those with malalignment, the ventriculoarterial connections were double outlet from the right ventricle, from the left ventricle, or were transitional with overriding of one of the great arteries. In the clinical series, 19 of 35 patients (54%) in whom the aorta arose from the morphologically right ventricle underwent either myectomy to enlarge the interventricular communication or a Damus-Kaye-Stansel anastomosis was fashioned to treat existing or potential subaortic stenosis. Only 1 of 8 patients with the aorta arising from the dominant ventricle needed similar surgical procedures.
Conclusions: Ventriculoarterial connection in double inlet left ventricle demonstrated a morphologic spectrum and needs precise recognition to provide an unobstructed ventricular outflow after operation.
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Introduction
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In the setting of double inlet left ventricle, discordant ventriculoarterial connection is commonly seen in hearts with a hypoplastic and incomplete morphologically right ventricle on the left side (the so-called SLL type) [1–3], whereas a concordant ventriculoarterial connection, which is a vital element for the so-called Holmes heart, is less common [4, 5]. A small proportion of hearts with double inlet left ventricle have some other manner of ventriculoarterial connections, such as double outlet from the right or the left ventricle [6, 7]. Accordingly, we investigated a combined series of hearts with this entity, in postmortem specimens and in patients, focusing on ventriculoarterial connections to determine precisely the morphologic spectrum and to consider implications for options available for surgical procedures.
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Material and Methods
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This retrospective study was approved by the Institutional Ethics Committee, and individual patient consents were waived.
We examined 54 autopsied heart specimens of double inlet left ventricle. Another consecutive series of 43 clinical patients were assessed on the basis of imaging as well as direct inspection during heart operations. All patients underwent an intracardiac operation, and none were included in the autopsied series. The type of definitive repair was ventricular septation in 22 and the Fontan type procedure in 19. One patient remained with the bidirectional Glenn physiology, and another patient with coarctation of the aorta underwent the Norwood type procedure.
In total, 96 had the usual atrial arrangement, and only 1 clinical patient possessed its mirror imagery. This exceptional case was described as seen in a mirror so that we could correlate it with the other cases. The incomplete and hypoplastic morphologically right ventricle was located anteriorly and to the left of the dominant left ventricle in 62, but rightward and adjacent to the right atrium in 35.
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Results
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The morphologic features around the ventriculoarterial connection are summarized in Table 1.
Common Types
Of 62 with the right ventricle leftwards, 46 (74%) had the SLL type, in which the left-anteriorly located ascending aorta originated entirely from the morphologically right ventricle with the pulmonary trunk (right posterior) entirely from the dominant left ventricle (Fig 1). Of 35 with the right ventricle rightwards, 13 (37%) had the Holmes heart, with the normally related great arteries with concordant ventriculoarterial connection, and 15 (43%) had discordant ventriculoarterial connection with the aorta located right anteriorly to the pulmonary trunk (Fig 2).
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Fig 1. Diagrams of ventriculoarterial connections in patients and specimens with double inlet left ventricle with the right ventricle leftwards in relation to the dominant left ventricle. The schemas are drawn as seen from the top. The numbers of examples are shown adjacent to each schema. Percentages indicate degree of overriding of the aorta. (Ao = aorta; LV = morphologic left ventricle; PA = pulmonary arterial trunk; RV = morphologic right ventricle; VA = ventriculoarterial connection.)
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Fig 2. Diagrams of ventriculoarterial connections in patients and specimens with double inlet left ventricle with the right ventricle rightwards and adjacent to the right atrium. The schemas are drawn as seen from the top. The numbers of examples are shown adjacent to each schema. Percentages indicate degree of overriding of either the aorta or the pulmonary trunk. (Ao = aorta; PA = pulmonary arterial trunk; RV = morphologic right ventricle; LV = morphologic left ventricle; VA = ventriculoarterial connection.)
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Atypical Patterns in Hearts With the Right Ventricle Leftwards
Four (6%) had discordant ventriculoarterial connections but with unusual aortopulmonary orientations (Fig 1); the aorta was to the left of the pulmonary trunk in a side-by-side fashion in 2 or was right-anteriorly located in 2. The outlet septum in these 4 hearts was in alignment with the muscular ventricular septum; in another 4, the outlet septum was malaligned (posteriorly oriented in relation to the muscular ventricular septum). Because of that, the aorta was overriding the left ventricle by 25% in 2, by 50% in 1, or exclusively arising from the left ventricle in the remaining 1. In these hearts the aorta was anterior or left anterior to the pulmonary trunk. No heart had a concordant ventriculoarterial connection when the aorta was located anteriorly to the pulmonary trunk; this particular situation is known as a part of the features that are seen in the so-called anatomically corrected malposition.
In one heart in which the aorta was located to the right and side-by-side to the pulmonary trunk, both great arteries arose entirely from the incomplete and hypoplastic morphologic right ventricle. The outlet septum was unequivocally malaligned with the muscular ventricular septum. In another 2 with the aorta normally orientated relative to the pulmonary trunk, the ventriculoarterial connection was concordant, and there was no malalignment of the outlet septum. These 2 hearts had a regular spiraling arrangement of the great arteries.
In the remaining 6 hearts (10%), there was pulmonary atresia, with the aorta arising entirely from the morphologic right ventricle, including 1 with an imperforate pulmonary valve (Fig 3). The remnant of the pulmonary trunk suggested a left anterior orientation of the aorta in 5 and right side-by-side in 1.
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Fig 3. (a) An example of both great arteries arising from the right-sided morphologic right ventricle. The ventricular septal defect is large, and the outlet septum is oriented perpendicular to the muscular ventricular septum. Panels b, c, and d show examples of unusual ventriculoarterial connections; the aorta arising from the morphologically right ventricle and the pulmonary pathway having membranous atresia. (b) The aorta was anterior to the pulmonary trunk, and the arterial trunks had a parallel arrangement. (c) From the dominant morphologic left ventricle, the imperforate pulmonary valve was seen in relation to the crest of the muscular ventricular septum, while the forceps through the aortic valve indicated that the aortic valvar orifice exclusively originated from the morphologic right ventricle. The outlet septum was markedly attenuated. (d) This view from the pulmonary trunk revealed an imperforate pulmonary valve. (Ao = aorta; AoV = aortic valve; AVV = atrioventricular valve; PT = pulmonary arterial trunk; PV = pulmonary valve; RA = right atrium; RV = morphologic right ventricle.)
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Atypical Patterns in Hearts With the Right Ventricle Rightwards
The aorta was to the right of the pulmonary trunk in a side-by-side fashion in 3 hearts (Fig 2, lower row). Although the aorta originated entirely from the right ventricle, the pulmonary trunk was entirely from the right ventricle (double outlet right ventricle; Fig 3), with 25% overriding the dominant left ventricle or entirely from the left ventricle (discordant ventriculoarterial connection).
In another example, the aorta was left and side-by-side to the pulmonary trunk, and 50% overriding to the dominant left ventricle with the pulmonary trunk arising from the right ventricle. In one case with right-anterior aorta, the aorta was overriding by 25% to the right-anterior right ventricle (Fig 2, in the middle pane).
Two hearts had an atretic pulmonary trunk, with the aorta arising from either the right or the left ventricle. The remnant of the pulmonary trunk indicated the potential orientation of the great arteries as seen in the common patterns for hearts with the right ventricle rightwards.
Ventricular Outflow Tracts in the Clinical Series
Obstruction of the aortic arch coexisted in 5 (coarctation in 4 and interruption in 1) of 43 clinical patients (12%). In 4 the right ventricle was leftwards and there was a discordant ventriculoarterial connection (the common SLL type), and the ventricular outflow tract to the aorta was narrow owing to restriction at the level of the interventricular communication (Fig 4). In the remaining patient, the right ventricle was rightwards and adjacent to the right atrium, and the ventriculoarterial connection was transitional between the discordant and entire double outlet left ventricle. The interventricular communication did not appear to be an ultimate restrictive factor for the flow to the aortic channel.
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Fig 4. Diagrams of obstructions across the aortic or pulmonary pathway in clinical patients. A solitary arrow indicates a restrictive interventricular communication. A broken arrow indicates deviation of the outlet septum. A dual arrow shows a markedly deviated and substantially formed outlet septum. Aortic pathway obstruction includes coarctation of the aorta, interruption of the aortic arch, or subaortic stenosis. (Ao = aorta, LV = morphologic left ventricle; PA = pulmonary arterial trunk; RV = morphologic right ventricle; VA = ventriculoarterial connection.)
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Pulmonary stenosis was seen in 17 (40%), of whom 15 had discordant ventriculoarterial connections; 11 with the right ventricle leftwards and 4 with the right ventricle rightwards (Fig 4). The pulmonary valve orifice was squeezed between the outlet septum and the atrioventricular valves. In the other 2 with the right ventricle rightwards and concordant ventriculoarterial connection, the interventricular communication was restrictive to the pulmonary pathway. Pulmonary atresia was present in 2 patients with the right ventricle leftwards, and the aorta originated from the morphologic right ventricle.
The aorta was arising from the morphologic right ventricle in 28 of 29 patients with the right ventricle leftwards and in 6 of 14 patients with the right ventricle rightwards. Of these, 19 (56%) underwent surgical maneuvers, by either myectomy at the level of the interventricular communication or additional aortopulmonary anastomosis (the Damus-Kaye-Stansel anastomosis), to treat existing or potential subaortic stenosis (Fig 5). These included the 4 patients with obstruction of the aortic arch, 6 of 14 with no aortic coarctation or pulmonary stenosis (including 1 with double outlet right ventricle), 8 of 15 with pulmonary stenosis, and 1 of 2 with pulmonary atresia.
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Fig 5. Diagrams of ventricular outflow tracts in clinical series in relation to outflow obstructions and surgical procedures used to avoid subaortic stenosis (by either the Damus-Kaye-Stansel anastomosis or enlargement of the interventricular communication). A set of the numbers indicates the number of the surgical procedures used for this purpose from the total number of each pattern of ventriculoarterial connection. Aortic pathway obstruction includes coarctation of the aorta, interruption of the aortic arch, or subaortic stenosis. (Ao = aorta; LV = morphologic left ventricle; PA = pulmonary arterial trunk; RV = morphologic right ventricle.)
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In the exceptional patient with the right ventricle leftwards, the ascending aorta was oriented left anteriorly to the pulmonary trunk. We initially presumed the ventriculoarterial connection was a double outlet right ventricle because of the presence of hypertrophied muscular trabeculations, but it turned out to be a double outlet left ventricle. This patient underwent banding of the pulmonary trunk as a first palliation, and we very cautiously monitored this patient until the next stage of surgical procedure; we anticipated progression of subaortic stenosis to a greater or lesser degree. Nonetheless, on ventriculography before the Fontan type procedure, we confirmed the presence of a rudimentary ventricle of the morphologic right type located leftwards, but it was not related to either of the great arteries. No subaortic narrowing has been noted for 9 years after the Fontan completion.
Only 1 of 8 patients with the right ventricle rightwards and the aorta arising mainly from the dominant left ventricle underwent surgical treatment for moderate subaortic stenosis. This patient's aorta was anterior to the pulmonary truck, and coarctation of the aorta was repaired during the neonatal period and the pulmonary trunk was banded. We regarded this patient also as a high-risk case for progressive subaortic stenosis; but contrary to our expectation, the subaortic region remained unobstructed. We subsequently inspected the subaortic channel through the aortic valve and through the atrial incision at the time of total cavopulmonary connection and noted a mild degree of overriding of the aorta (by 25%) to the small morphologic right ventricle. Because of the malalignment between the muscular ventricular septum and the outlet septum, the pathway to the aorta appeared sufficiently wide, and we did not use surgical maneuvers such as the Damus-Kaye-Stansel anastomosis or enlargement of the interventricular communication.
Nine years later, nonetheless, the pressure gradient between the dominant left ventricle and the ascending aorta was 37 mm Hg by catheter measurement. Although the degree of obstruction was moderate, there was a progressive decrease in ventricular contraction. The patient consequently underwent reoperation with excision of the outlet septum and removal of musculature from the crest of the ventricular septum. The pressure gradient dropped to 4 mm Hg during the procedure.
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Comment
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Stereotypes of double inlet left ventricle have been documented mainly by location of the hypoplastic and incomplete morphologic right ventricle (either rightwards or leftwards) in relation to the dominant morphologic left ventricle, as well as concordant or discordant ventriculoarterial connections [7]; namely, two multiplied by two equals four essential stereotypes. The combination of the right ventricle leftwards and concordant ventriculoarterial connections is known to be exceedingly rare [7] and was seen in 2 of the 97 examples of this study. The commonest stereotype is clinically known as the SLL type, which is a small and incomplete morphologic right ventricle being left-anteriorly located to the dominant morphologic left ventricle, with discordant ventriculoarterial connections in which the ascending aorta arises left anteriorly to the pulmonary trunk. It is well recognized that the interventricular communication frequently causes subaortic stenosis in this setting [8–10]. Historically, it is known that Holmes described in 1824 the concordant ventriculoarterial connection with double inlet atrioventricular connection to the left ventricle and the right ventricle rightwards (a small and incomplete morphologic right ventricle located right anteriorly to the dominant morphologic left ventricle) [4].
This "quartet" classification of morphologic spectrum is pertinent because tricuspid atresia is considered under a similar concept [11]. When we find an example of tricuspid atresia with double outlet right ventricle [12, 13], however, we question whether the quadradivision is adequate. As we have documented, unusual ventriculoarterial connections can have clinical relevance. In the patient who initially had coarctation of the aorta and eventually underwent relief of subaortic obstruction after the Fontan completion, perhaps, intervention to the ventricular outflow tract could have been applied earlier and prophylactically. The Damus-Kaye-Stansel anastomosis in this setting [14–16] could be over-indicated even in those who do not have eventually the potential for developing subaortic stenosis. Nonetheless, this remains debatable: The additional maneuver should better be avoided, if not really needed, because of another possible compromising factor, which is regurgitation across the semilunar valve additionally placed for the systemic circulation [17].
On the other hand, when the aorta and the pulmonary trunk both arise from the rudimentary and morphologic right ventricle that lacks an inlet component, the addition of an aortopulmonary anastomosis is unsuitable for relieving subaortic obstruction. Only enlargement of the interventricular communication can resolve the obstruction. Previously accumulated knowledge is of great help to avoid injury to the conduction bundle when the ventricular septum is incised [18], irrespective of ventriculoarterial connections.
These special considerations would not have been required in most hearts with double inlet left ventricle because the ventriculoarterial connections were of typical patterns in four-fifths of our series. Still, we should not ignore the remaining patterns, albeit uncommon, seen in a fifth of examples. Orientation of the great arteries was not predictive of the precise types of ventriculoarterial connections. An atypical ventriculoarterial connection can be present with usual orientation of the great arteries, whereas a common type of ventriculoarterial connection (concordant or discordant) may be the case with the aorta and the pulmonary trunk unusually located. The percentage of less typical variants appeared slightly higher than previously documented in the established textbook of cardiac surgery [6]. This probably reflects the background nature of the present materials, which is based on both clinical patients and autopsied specimens.
We also observed that there were transitional spectrums between concordant or discordant connections and double outlet right or left ventricle. Albeit a quadrapolar scheme is theoretically more precise than concordant-discordant resolution in the ventriculoarterial connection, overriding of one of the great arteries needs recognition. To note whether overriding is present, malalignment between the outlet septum and the muscular ventricular septum, as well as orientation of the aorta relative to the pulmonary trunk, must be described. These perceptive points are also of practical use in patients with pulmonary atresia. In this particular setting, the aorta frequently originated from the morphologic right ventricle (7 of 8 cases). The size and shape of the outlet septum and the degree of alignment of the structure to the rest of the ventricular septum vary. Whether the aortic pathway is potentially obstructive depends on the size of the interventricular communication. The presence of pulmonary atresia does not necessarily imply an unobstructed subaortic channel.
An obvious limitation of this study is the lack of physiologic consideration. It has been well documented that the size of the interventricular communication changes depending on the volume load conditions to the ventricles [9, 10, 16, 19]. Even in a typical double inlet left ventricle with the right ventricle leftwards and discordant ventriculoarterial connections, subaortic stenosis might not progress if the communication was truly large in diameter [6]; whereas, for example, 50% overriding of the aorta to the dominant left ventricle could have obstruction across the systemic ventricular outflow tract if the aortic orifice was notably small. In this respect, further quantitative analyses are needed. We nevertheless focused in the present study on morphologic and qualitative aspects to highlight atypical variants of ventriculoarterial connections that can exist in double inlet left ventricle and require careful assessment before deciding on optimal surgical strategy.
Besides the typical forms of double inlet left ventricle with discordant or concordant ventriculoarterial connection, less frequent but important patterns were present that had surgical relevance for ventricular outflow obstruction. The four headings of concordant, discordant, double outlet right, double outlet left, and the transitional spectrums between these require recognition. When the aorta arises from the morphologic right ventricle, the subaortic channel requires particular attention for potential obstruction.
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Acknowledgments
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Hideki Uemura was working at the National Cardiovascular Center of Japan between May 1988 and March 2004 when part of this study was done.
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References
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Invited Commentary
- Robert H. Anderson
Ann. Thorac. Surg. 2008 86: 1327.
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R. H. Anderson
Invited Commentary
Ann. Thorac. Surg.,
October 1, 2008;
86(4):
1327 - 1327.
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Abstract
Introduction
