J Thorac Cardiovasc Surg 2006;132:640-646
© 2006 The American Association for Thoracic Surgery
Surgery for Congenital Heart Disease |
Late incompetence of the left atrioventricular valve after repair of atrioventricular septal defects: The morphologic perspective
Mazyar Kanani, MRCSa,*,
Martin Elliott, MD, FRCSa,
Andrew Cook, PhDa,
Amy Juraszek, MDb,
William Devine, BSc,
Robert H. Anderson, MD, FRCPatha
a Cardiac Unit, Great Ormond Street Hospital for Children, London, UK
b Cardiac Registry, Department of Pathology, Harvard Medical School, Children's Hospital, Boston, Mass
c Department of Pathology, University of Pittsburgh Medical School, Children's Hospital of Pittsburgh, Pittsburgh, Pa.
Received for publication July 6, 2005; revisions received January 13, 2006; accepted for publication January 30, 2006.
* Address for reprints: Mazyar Kanani, MRCS, Cardiac Unit, Great Ormond Street Hospital for Children, Great Ormond Street, London WC1N 3JH, UK (Email: mazzykanani{at}hotmail.com).
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Abstract
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OBJECTIVE: The mortality following repair of atrioventricular septal defects has fallen dramatically in the last 4 decades, but reoperation for late regurgitation across the left atrioventricular valve has remained disconcertingly stagnant. Seeking potential structural causes, we compared the morphology of the surgically created septal leaflet of the left valve following repair of atrioventricular septal defects to the aortic leaflet of the normal mitral valve.
METHODS: We compared the mitral valves of 92 normal hearts to the left ventricular components of the bridging leaflets of hearts with atrioventricular septal defect with common atrioventricular junction, determining the shape of the leaflets and the arrangement of the subvalvar apparatus.
RESULTS: The aortic leaflet of the mitral valve is triangular compared with its rectangular septal counterpart after repair of atrioventricular septal defect. The cordal arrangement in the mitral valve is well organized, compared with the deficient cordal arrangement of the abnormal valve. A greater proportion of cords in the mitral valve divide to 3 generations (55.5% compared with 8.7%; P < .001), and a higher percentage of cords remain undivided in atrioventricular septal defects (60.8% compared with 25%; P < .001).
CONCLUSIONS: Not only is the annular component in the left atrioventricular valve abnormal, but the subvalvar apparatus is characterized by deficiency and disarray. Furthermore, the axis of cordal insertion may potentiate to separation over the long term of the leaflets joined surgically. Valvar repair in this setting will never restore the arrangement of the normal mitral valve.
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Introduction
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In this present era of repair of atrioventricular septal defects with common atrioventricular junction, or atrioventricular canal, attention has veered from early mortality as the best measure of operative success and focused onto the long-term quality of life subsequent to surgical repair. This is commonly measured in terms of exercise ability and freedom from reoperation for residual lesions. Of these latter problems, the most common and troublesome is progressive regurgitation across the newly created left atrioventricular valve, occurring even if the repair was considered robust initially.
The key to the durability of this trifoliate valve is the zone of apposition between its bridging leaflets. Despite the belief that complete closure of this zone is the single, and best, way of ensuring competence, the rate of reoperation has remained disconcertingly stagnant over the last 30 years. Why should this be? The reasons are probably multifactorial, but to help provide some insights, we have returned to first principles and compared the structure of the surgically created septal leaflet of the left valve in atrioventricular septal defects with its normal counterpart, the aortic leaflet of the mitral valve. Our findings illustrate why this surgically created leaflet will, from the morphologic perspective, always remain the Achilles' heel of surgical repair, even in the best hands.
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Methods
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We analyzed 92 normal hearts from the Cardiac Registry of the Children's Hospital, Boston, Massachusetts, together with 72 hearts with atrioventricular septal defect with common atrioventricular junction. The latter were selected from 200 specimens studied in the Cardiac Archive, Great Ormond Street Hospital, London (28 hearts); The Frank E. Sherman, Cora C. Lenox Heart Museum, Children's Hospital of Pittsburgh, Pennsylvania (30 hearts); and the Cardiac Registry, Children's Hospital, Boston, Massachusetts (14 hearts). We examined only those with an intact left atrioventricular valve. Of those chosen for further study, 26 had separate valvar orifices, the so-called "ostium primum defect," with the remaining 44 possessing a common valvar orifice.
In the normal hearts, we studied the morphologic features of the aortic leaflet of the mitral valve. In the hearts with atrioventricular septal defect with common atrioventricular junction, we analyzed the left ventricular components of the superior and inferior leaflets bridging the ventricular septum. We analyzed 32 hearts that had been repaired surgically and 40 in which surgery had not been performed. We excluded from consideration any specimens deemed retrospectively to be unsuitable for biventricular repair, such as those with a small left ventricle and those with a solitary left ventricular papillary muscle. Similarly, we excluded from consideration any hearts with accessory orifices in the left atrioventricular valve.
We took particular note of:
The shape of the leaflet, comparing the aortic leaflet of the normal mitral valve with the components forming the septal leaflet of the left atrioventricular valve subsequent to surgical repair of atrioventricular septal defect.
The arrangement of the tension apparatus at the ventricular surface of the leaflet.
The pattern of division of the tendinous cords as they arise from the papillary muscles.
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Statistical Analysis
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The degree of cordal division was expressed as the median and range. A Poisson regression analysis was performed in order to compare the incidence of undivided tendinous cords and cords that divide to the third generation.
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Results
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Shape of the Leaflet
The aortic leaflet of the mitral valve is uniformly triangular (Figure E1, left panel). The base of this triangle is continuous, via the area of fibrous continuity, with the left and noncoronary leaflets of the aortic valve, being thickened at each end as the right and left fibrous trigones. Despite this broad base, the aortic leaflet of the mitral valve guards only about one third of the overall annular circumference of the left atrioventricular orifice. Tendinous cords merge along the entirety of the sloped sides of the triangle, diverging away from either side of the leaflet to insert into their respective papillary muscles (Figure 1).
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Figure E1. Schematic representation of the aortic leaflet of the mitral valve (left panel) and neoanterior leaflet of the left atrioventricular valve in repaired atrioventricular septal defect with common atrioventricular junction (right panel). In the mitral valve, the aortic leaflet is triangular in shape, with the base continuous with the aortic valve through the region of valvar fibrous continuity. Tendinous cords emerge from the sides to insert into the papillary muscles on either side of the left ventricular outflow tract. The neoanterior leaflet is relatively larger than the mural leaflet and is rectangular, with a central alcove for the mural leaflet. The base of the rectangle relates to the ventricular septum, forming the artificial component of the annulus. Tendinous cords run in the longitudinal axis of the leaflet to insert into papillary muscles plastered to the parietal wall of the ventricle.
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Figure 1. Photographs of the ventricular surface of the aortic leaflet of the mitral valve. There is an orderly and radial arrangement to the tendinous cords. The close-up view of another heart (right panel) reveals that many of these cords divide as they arise from the papillary muscle, giving the ventricular surface a laminated appearance. The leaflet is continuous with the aortic valve (AV).
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The newly created septal leaflet of the repaired left atrioventricular valve in hearts with atrioventricular septal defect forms a coapting surface with its smaller counterpart, the left mural leaflet, with the latter guarding less than one third of the newly created left atrioventricular annulus. When the left ventricular components of the bridging leaflets have been surgically united, a bipartite leaflet is created that is more rectangular, with a triangular recess in its center that apposes the mural leaflet (Figure E1, right panel). This septal leaflet forms an antiparietal component that is a composite of different structures, depending on the mode of surgical septation. Specifically:
Following the two-patch repair, the annulus of the left atrioventricular valve is composed, in part, by leaflets sandwiched between the septal patches.
After the single-patch technique, the annulus is composed of the solitary patch, with the septal leaflet sutured to its surface.
Following the modified single-patch technique, the leaflet is sandwiched between the crest of the ventricular septum and the septal patch.
In the case of atrioventricular septal defect with separate valvar orifices, the base of the leaflet has the atrial patch above, the bridging leaflets themselves being adherent to the ventricular septal crest.
The Arrangement of the Tension Apparatus
The papillary muscles in the normal heart are located on either side of the left ventricular outflow tract, beneath the two ends of the solitary zone of apposition between the aortic and mural leaflets. Tendinous cords radiate from the ventricular surface of the leaflet to their respective papillary muscle. Marked consistency is found in this cordal arrangement. Although the cords have different destinations on the leaflet, in many instances they are branches of the same cord emerging from the papillary muscle. Typically, as the cord arises from the muscle, it divides into three successive generations that insert progressively and more deeply into the rough zone. The first generation merges into the free edge, the second generation into the ventricular surface more toward the annulus, with the third generation inserting into the ventricular aspect of the leaflet as the thick strut cord (Figure E2). Cords may also insert directly into the leaflet without division, but these account for a significantly smaller population of cords, with a median of only 25.0% and a range from 0% to 50% of the total cords, compared with those dividing thrice, which have a mean of 55.5% and a range from 20% to 100%.
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Figure E2. The division of the tendinous cords in the normal mitral valve. The majority of cords divide into strut and free-edge components that blend into the fabric of the leaflet. During systole, the force along the entire length of the leaflet is directed down a single cord (middle panel). This enables a single cord to support the entire length of leaflet. The right panel shows this division in reality.
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This pattern of cordal division and insertion produced a consistent organization of the ventricular surface of the aortic leaflet itself, giving it a distinctive appearance among all the valves examined. At the point of insertion, the cord broadened and blended with the leaflet. Because there was a maximum of three generations of division for each cord arising from the papillary muscle, the combination of broadening and layered cordal insertion produced a trilaminar configuration for the ventricular surface, with each layer being continuous with the expanded distal ends of the cords (Figure 1).
Compared with the mitral valve, the cordal arrangement of the surgically created septal leaflet in atrioventricular septal defects with common atrioventricular junction was more variable. In atrioventricular septal defects, the cords ran in the longitudinal axis of the septal leaflet (Figure E1, right panel, and Figure 2). The cordal axis, therefore, was also perpendicular to the ventricular septum. At the subvalvar level, the cords were disorganized compared with the mitral valve, the cords being relatively deficient, variable in thickness, and fusing in variable fashion with the underside of the leaflet. In 20 of the 26 hearts with separate orifices (77%), they were variably fused to the base of the leaflet. This type of cordal fusion was seen in 30 of the 44 hearts examined with a common valvar orifice (68%). On other occasions, the leaflet was attached directly to the papillary muscle, with no cords seen on the ventricular aspect of the potential septal leaflet (Figure E3); this feature was more frequent in hearts with separate valvar orifices. Compared with the mitral valve, a greater proportion of the total cordal population remained undivided, with a median of 60.8% and a range from 10% to 100%, with fewer cords dividing to the third generation, giving a median 8.7% of the total cords and a range from 0% to 75% (P < .001; Figures 3 and 4).
This greater population of undivided cords produced a distinctly unilaminate arrangement when compared with the trilaminate aortic leaflet of the mitral valve.
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Figure 2. Photographs of 2 examples of the subvalvar arrangement of the neoanterior valve in atrioventricular septal defects. In the left panel, the bridging leaflets have been closed with pledgets and in the right panel with unpledgeted sutures. There is cordal disorganization in both examples with a greater degree of cordal fusion beneath the right example. Compare this with the normal mitral valve, which conforms to a specific design with little morphologic variation. The 5-pointed arrow marks the superior papillary muscle, which has fused directly with the base of the superior bridging leaflet.
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Figure E3. Closer views of the subvalvar arrangement beneath the superior bridging leaflet of atrioventricular septal defects with a common valvar orifice. The example on the left shows cordal fusion. The right panel shows abnormal cordal forms and cordal tags, together with central cordal absence. LVOT, left ventricular outflow tract; SPM, superior papillary muscle.
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Figure 3. Box plot of the percentage of tendinous cords that divide to the third generation. In the mitral valve, a median of 55.5% of cords divide to the third generation, compared with the left atrioventricular valve in atrioventricular septal defects where a median of 8.7% of cords divide to the third generation (P < .001 at 95% confidence interval). AV, aortic valve.
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Figure 4. Box plots demonstrating the percentage of cords found that remain undivided. In the atrioventricular septal defect, a median 60.8% of the cords remain undivided, compared with 25% in the mitral valve (P < .001 at 95% confidence interval). AV, aortic valve.
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Discussion
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The mitral valvar complex is well designed for the task of maintaining atrioventricular competence across all physiologic loading conditions. The annulus forms a D-shaped flexible ring that contracts during systole, permitting the 2 leaflets to coapt firmly along a solitary zone of apposition.1,2 The leaflets are folded at their free edges to form a coapting surface that interlocks with its counterpart. The integrity of the subvalvar apparatus, consisting of the tendinous cords and papillary muscles, is crucial to coaptation during the cardiac cycle. The nature of division of these cords suggests that their activity is coordinated. It is possible to distinguish three types of cords: those inserting to the free edge of the leaflets, strut cords that insert into the ventricular surface, and the basal cords that originate from the ventricular wall and insert into the ventricular surface of the mural leaflet close to the annulus.3 Although it is known that the cords supporting the free edge, also known as marginal or first order cords, are vital to coaptation, there has been recent interest in the "strut" or "stay cords." These have been likened to stabilizing cables.4 It has previously been observed that there are up to 4 such cords supporting the aortic leaflet of the mitral valve,5 each being vital to the maintenance of left ventricular geometry and global function,6 with deleterious effects to systolic function if divided7 without affecting leaflet coaptation and valvar competence.8
Thus, although cords have been well described with respect to their final destination into the leaflet3 and the physiologic properties of each type of cords have been analyzed closely,7–10 we have shown that they are often branches of the same principle cord at the papillary muscle (Figures 1 and E2). We contend that the thick strut cord is a direct and linear continuation of this principle cord, consistent with previous observations,11 but that crucially, the so-called first-order cords may also arise from this thicker cord, but at a more acute angle, enabling them to reach the edge of the leaflet. Thus, although these two cordal forms could not be any more different in their size, position, and function, we have observed that they usually arise from the same "parent" cord at the level of the papillary muscle. Furthermore, once generated, these cords insert in a manner that confers a layered appearance to the leaflet (Figure 1).
The observation of common cordal origins, together with confirmation of a conserved and layered arrangement to the mitral leaflet, emphasizes the notion that the components of the valve work as an integrated unit and that altering the form of 1 component may compromise the function of another. It also begs the question about the physiologic advantage of this laminar arrangement. Conceivably, it may permit the greatest and most efficient support for any given population of cords. Thus, each cord from the papillary muscle, through generational division, may support the entire length of the leaflet from the annulus to the coapting edge, with a more even distribution of tensile strength along the leaflet canopy (Figure E2). The radial arrangement of the layered insertion may also aid in evenly distributing forces across the area of the canopy, limiting the burden on any individual area. For this reason, we believe that, physiologically, cords must not be considered in terms of isolated subtypes, but rather that each cord must be considered as an integrated unit consisting of strut and free edge components within a greater organization at the ventricular surface of the leaflet. The leaflets themselves consist of rigid fibrous material, with little inherent ability to stretch. Despite this, they are required to form a competent and flexible canopy. The layered arrangement may permit the leaflet to attain greater flexibility and extensibility than a unilaminate sheet. These physiologic contentions are presently conjecture in the absence of in vivo experimentation but nonetheless conceivable in the light of our observations and what is already known of valvar physiology.
This conserved arrangement is lost in the setting of the newly created septal leaflet in the repaired left valve of the atrioventricular septal defect with common atrioventricular junction. Not only is the branching pattern less complex than the normal, but dysplastic cords extend perpendicular to the long axis of the leaflet. The trilaminar arrangement characterizing the aortic leaflet of the mitral valve is also absent. Consequently, the newly created septal leaflet takes the form of a more rigid structure, with potentially reduced ability to adapt to changing physiologic conditions. Fearing this rigidity, earlier surgeons had suggested that the zone of apposition between the left ventricular components of the bridging leaflets be left unclosed.12 Added to this is the marked difference in annular component, a common structure in the setting of the atrioventricular septal defect, which differs markedly from the arrangement seen in the normal mitral valve. Any deficiency of the leaflets themselves may further expedite valvar incompetence, as has been seen in situations where the inferior bridging leaflet is smaller than expected.13
Why does the zone of apposition reopen with time? At reoperation for left atrioventricular incompetence, the regurgitation is usually seen through the distal end of the zone of apposition, where the bridging leaflets have started to disconnect (Figure E4). To help understand this phenomenon, we must ask whether the gap permitting regurgitation represents a true cleft within the valve, comparable to the so-called isolated cleft of the otherwise normal mitral valve, or whether it is a zone of apposition between two of the leaflets of a trifoliate valvar structure.14 Closer examination reveals that it is neither. The ends of the solitary zone of apposition between the 2 leaflets of the normal mitral valve conform to a very specific pattern, being supported by fan-shaped commissural cords3 (Figure E5, right panel). Thus, all of the tension on the ends of the zone of apposition during ventricular systole is coordinated down a single cord, making the system very efficient (Figures 5, a, and E5, right panel). In comparison, although the left ventricular components of the bridging leaflets in hearts with atrioventricular septal defect do meet along a zone of apposition, the components of this zone are almost completely unsupported in terms of cordal attachment and lack the features of the normal "commissure" (Figure E5). Following surgical closure of the zone at operation, cords diverge from one another to insert into their respective papillary muscles and then support the tip of the newly created septal leaflet. During loading conditions, the direction of the force, therefore, separates the leaflets (Figure 5, b). This is also true of the aortic leaflet of the mitral valve, where the cords diverge at the tip of the triangular leaflet, but in the latter setting, there is no artificial suture line acting as a chronic point of weakness.
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Figure E4. Photograph of the neoanterior leaflet several years after the repair of a common atrioventricular junction with a common valvar orifice. The superior and inferior bridging components of the valve have separated at the tip of the leaflet, causing regurgitation. This may be encouraged by the manner in which the tendinous cords diverge away from the line of closure to insert into their respective papillary muscles.
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Figure E5. The unrepaired zone of apposition in atrioventricular septal defect with separate valvar orifices (left panel) compared with the commissure between the aortic and mural leaflet in the normal mitral valve (right panel). The zone of apposition forms an unsupported commissure between the bridging leaflets. In this example, taken from a neonatal heart, the bridging leaflets are totally bereft of cordal support. The commissure of the mitral valve is always supported along its entire length by a solitary cord that divides into multiple free-edge cords. SBL, superior bridging leaflet; IBL, inferior bridging leaflet; VS, ventricular septum; AL, aortic leaflet; ML, mural leaflet.
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Figure 5. A schematic representation of the forces at work on the mitral commissure (a) and the neoanterior leaflet in atrioventricular septal defects (b). In the mitral commissure, the stress force from the length of the commissure is conceivably directed down the solitary cord, providing the most efficient mechanism, also seen in Figure E5 (right panel). Closure of the zone of apposition in atrioventricular septal defects never attains the normal commissural arrangement as the stress forces on the cords diverge to their respective papillary muscles, producing a tendency for the leaflets to separate. In order to achieve the normal commissural distribution of force, extended zonal closure may have to be undertaken (c). This may reduce the stresses on the zone of apposition suture line by directing some of the force inferiorly instead of laterally, but may lead to left atrioventricular valvar stenosis. AML, aortic mitral leaflet; MML, mural mitral leaflet.
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One way to repair the zone in order to distribute the forces like the normal "commissure," taking the stresses off the tip of the leaflet, may be to perform an extended closure where the cords are sutured together beneath the zone of apposition (Figure 5, c). Alternatively, cords may be transferred from the mural leaflet to the tip of the zone of apposition to restore, in part at least, the normal mechanism of support.12,15 This may be practically and technically impossible, given the ever-present risk of creating valvar stenosis. It is because this zone is, in effect, an unsupported commissure that surgeons seek, whenever possible, to close fully the zone of apposition. Although the zone may be secure in the short term, this lack of support promotes long-term incompetence. The importance of restoring the normal commissural arrangement was advocated by Carpentier,12 through additional surgery to the annulus and tension apparatus. Compounding this chronic tendency for separation of the leaflets is progressive dilation of the composite artificial annulus. Consequently, regurgitation begets regurgitation in the face of increased stress on the suture line.
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Conclusions
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It is evident that, even with adequate closure of the zone of apposition following repair of atrioventricular septal defects, the surgeon can never recreate the normal mitral valve. From the outset, every component of the valvar apparatus deviates from the normal. The annulus is a composite structure, containing artificial components subsequent to the surgical repair, and the restored septal leaflet has altered geometry, with a rotated axis of closure. The subvalvar apparatus is characterized by deficiency, dysplasia, and disarray. Once closed, the forces generated by cords arranged in the longitudinal axis of the leaflet may paradoxically encourage reopening at the tip of the newly created leaflet, especially if there is already some annular dilation. All of these factors interplay to encourage the long-term failure of the valve despite initial competence. The great morphologic variability seen within this context may explain why some valves are more robust than others. Although we concede that morphologic studies involving hearts from patients who, of necessity, have died may always reflect a self-selected population at the more severe end of the scale, we nevertheless believe that these observations suggest that, irrespective of the quality of repair, the left atrioventricular valve has from the outset, all the morphologic substrates for long-term incompetence. A further question will relate to the differences between those hearts with trisomy 21 compared with those of normal karyotype. This was presently not possible given the incomplete data on karyotype, but will be a valid exercise in the future in order to determine if it contributes to any differences between long-term valvar function.
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Acknowledgments
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We thank the British Heart Foundation for supporting this study. We also thank Miss Gemma Price for the preparation of the illustrations.
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Footnotes
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Funded by the British Heart Foundation.
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Abstract
Introduction
