Ann Thorac Surg 2000;69:556-561
© 2000 The Society of Thoracic Surgeons
Original Articles
Anatomy of the muscular subpulmonary infundibulum with regard to the Ross procedure
Anna F. Merrick, FRCSa,
Magdi H. Yacoub, FRCSa,
Siew Yen Ho, PhDa,
Robert H. Anderson, MDa
a Departments of Paediatrics and Surgery, Royal Brompton Campus, National Heart and Lung Institute, Imperial College School of Medicine, London, England, United Kingdom
Address reprint requests to Dr Ho, Imperial College School of Medicine, Department of Paediatrics, National Heart and Lung Institute, Dovehouse St, London SW3 6LY, England
e-mail: yen.ho{at}ic.ac.uk
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Abstract
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Background. To clarify the precise anatomical relationship of the muscular subpulmonary infundibulum.
Methods. Eleven hearts were dissected, and microscopic sections taken through the arterial trunks of a 37- week-old fetus and of a neonate. The anatomy was also investigated during operative Ross procedures.
Results. The sinotubular junctions of the pulmonary and aortic roots cross obliquely. The leaflets of the pulmonary valve are lifted away from the ventricular septum by the free-standing subpulmonary infundibulum, whereas the aortic valve is deeply wedged between the atrioventricular junctions. The muscular infundibulum spirals around the aortic root, being longest below the right-facing aortic sinus and shortest below the left. The first septal perforating artery pierces the septum below the shortest part of the infundibulum, sometimes within a millimeter of the pulmonary valvar hinge, but a muscular sleeve lifts the pulmonary leaflets from the septal musculature.
Conclusions. The pulmonary valvar leaflets are supported entirely by free-standing musculature, having no direct relationship with the ventricular septum. This makes possible the Ross procedure.
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Introduction
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The Ross procedure [1] is assuming ever increasing importance in the armamentarium of the cardiac surgeon. It is self-evident that optimal results will best be achieved when surgeons have a full understanding of the complex structure and relationships of the muscular subpulmonary infundibulum. Surprisingly, consensus on the structure of this area is difficult to achieve even when studied carefully by gross anatomic dissection. Thus, in recent years, we ourselves have made such detailed dissections [2], as have the group of morphologists working in Leiden University [3]. It became clear, following a recent exchange of correspondence [4, 5], that although most of our observations are in harmony, potentially important differences remain in our understandings. So as to clarify whether these discrepancies are true differences in anatomic interpretation, or merely semantic problems, we have studied additional hearts and made more careful dissections of the crucial muscular support of the leaflets of the pulmonary valve, concentrating on those aspects most important for the cardiac surgeon. At the same time, we have taken the opportunity to clarify the status of the so-called tendon of the infundibulum [6], and to assess its functional significance, if any.
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Patients and methods
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Macroscopic
We studied 11 hearts, 5 from infants, 1 from a child, and 5 from adults, by making careful dissections of the aortic and pulmonary roots, working from distal to proximal until we exposed the entirety of the musculature of the subpulmonary infundibulum. We then assessed the extent of the muscular infundibular sleeve relative to the attachments of the leaflets of the pulmonary valve, taking particular note of the relationships to the septal perforating arteries. These specimens were additional to the hearts described by Lal and colleagues [6], which we reexamined. We also took note of the relationships between the arterial roots themselves, noting the location of any fibrous structures encountered between them. Particular care was taken at the level of the intercoronary commissures. The hearts were then further examined to establish whether a fibrous raphe was to be found within the infundibular musculature. All hearts, except the one with valvar aortic stenosis, came from individuals without any disease which might have distorted the anatomic arrangement of the outflow tracts.
Microscopic
We reexamined the transverse sections through the arterial trunks of the 37-week-old fetus prepared by Lal and colleagues [6], and studied an additional heart from a neonate. The sections were fixed and stained with elastic van Gieson. One heart had been sectioned in the transverse plane of the aorta, and the other in the transverse plane of the pulmonary trunk.
Studies in the operating room
One of us (MY) has performed at least 200 pulmonary autograft procedures during which he has noted the presence or absence of the fibrous link between the aorta and pulmonary trunk and its precise location, and studied the living anatomical relationships of the components of the aorta and pulmonary trunk.
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Results
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Macroscopic examinations
The normal arterial valves have three approximately equally sized leaflets suspended in the form of a coronet within the arterial root. Each root is made up of the three fibrous sinuses of Valsalva, supported by their underlying ventricular structures. The attachment of each valvar leaflet to the wall of the ventricular outflow tract is semilunar. It is this locus which produces the hemodynamic ventriculo-arterial junction. The most proximal part of each leaflet is attached to ventricular structures, but the more distal attachments are hinged within the arterial sinuses, so that the hinges of the valve cross the anatomic ventriculoarterial junction. This anatomic junction is the circular locus over which the walls of arterial sinuses are supported by the underlying ventricle. It differs in the right and left ventricles. This is because the right ventricle possesses a completely muscular infundibulum (Fig 1) whereas, in the left ventricle, over part of the valvar circumference, there is fibrous continuity between the leaflets of the aortic and mitral valves (Fig 2). In the aortic root, therefore, the hinges of the valvar leaflets are attached in part to muscular structures, and in part to the fibrous aortomitral curtain.
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Fig 1. The heart has been prepared to show the relationship of the arterial roots. The pulmonary trunk has been tilted away from the aorta to show the extent of the subpulmonary infundibulum, and the extreme groove (between arrows) between it and the aortic sinuses giving rise to the coronary arteries. The aorta is cut at the sinotubular junction. Note the "flask" or "onion" shape of the aortic root. The white and black arrow indicates the first septal perforating artery, and the dotted line shows the circular junction between the wall of the pulmonary trunk and the muscular infundibulum.
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Fig 2. This long axis through the ventricular outflow tract shows the sleeve of infundibular musculature that lifts the pulmonary valve away from the aorta. Note that the long axes of the two outflow tracts are at almost right angles to each other. The noncoronary leaflet of the aortic valve is in fibrous continuity with the leaflet of the mitral valve. (L, R = left and right coronary aortic sinuses.)
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The significant feature of the pulmonary root, emphasizing its distinction from the aortic root, is that its ventriculoarterial junction is completely muscular. Thus, the entire pulmonary valvar complex is lifted away from the base of the heart by the free-standing subpulmonary infundibulum (Figs 2, 3). The infundibulum, which is narrowest at the anatomic ventriculoarterial junction, rises obliquely from the right ventricle so that it is longest below the right-facing sinus, and shortest below the left (Fig 3). The musculature of the free-standing subpulmonary infundibulum is not rigid like the structures which support the aortic valve. Most of the infundibulum is the continuation of the right ventricular free wall. The remainder (that part which is proximal to the adjacent parts of the facing sinuses) is supported by the crest of the muscular ventricular septum, but is separate from the septum (Fig 4).
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Fig 3. The relationship of aortic and pulmonary roots viewed from the front of the heart. The point of contact of the aortic and pulmonary sinotubular junctions is indicated.
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Fig 4. The free standing subpulmonary infundibulum has been dissected away from the base of the heart at the lowest point of attachment of the valvar hinges. The arrow indicates the first septal perforating artery. Note the deep crevice between the remaining "septal" component of the infundibular sleeve and the base of the aorta.
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Overall, the arterial roots are "flask" or "onion" shaped, being narrowest at the top and bottom of the attachments of the valvar leaflets, and widest at the middle of the sinuses. At the top, the sinuses are separated from the tubular arterial trunks by the discrete annular sinutubular junctions. The most distal part of the leaflets, at their peripheral zones of apposition, are tethered tightly to these junctions.
The sinotubular junctions of the aorta and pulmonary trunks are directly adjacent to one another only at the top of the interleaflet triangles between the coronary sinuses of the aorta, and the adjacent sinuses of the pulmonary trunk (Fig 5). Because of the obliquity of the axes of the ventricular outflow tracts, the aorta and pulmonary trunk leave the heart almost perpendicular to one another. Because of the angulation, the sinotubular junction of the aorta crosses obliquely the right-facing pulmonary valvar sinus, and continues in relation to that part of the pulmonary trunk immediately above the left-facing sinus. The pulmonary sinotubular junction, in contrast, crosses obliquely first the left coronary arterial sinus of the aorta, and then that part of the aorta immediately above the right coronary aortic sinus (Fig 3). The adventitia of the aortic and pulmonary sinuses are held together by a thin layer of fibrofatty tissue, such that sharp dissection is required to separate their apposing surfaces. Small parts of the right and left coronary sinuses of the aorta, and the interleaflet triangle between them, are joined in this fashion with the right-facing sinus of the pulmonary trunk (Fig 6). The pulmonary trunk then arches posteriorly as it leaves the heart, roofing over the aortic origin of the left coronary artery and its bifurcation. The left anterior descending (interventricular) artery extends in the loose areolar connective tissue at the ventricular base, giving off the first septal perforating artery. This artery passes behind the proximal part of the free-standing sleeve of muscular subpulmonary infundibulum and enters the basal part of the ventricular septum, extending between the diverging anterosuperior walls of the left and right ventricles. The infundibulum supporting the left-facing pulmonary sinus can always be dissected in the autopsied hearts by a perpendicular cut taken below the most proximal part of the attachment of the pulmonary valvar leaflet (Fig 7). The length of muscular infundibulum thus removed, nonetheless, varies from heart to heart. A small part of the proximal right coronary artery is related to the right-facing pulmonary sinus. The major part of the right coronary aortic sinus, however, is related to the subpulmonary infundibulum. The right coronary artery arising from the sinus curves round the infundibulum, encased in a layer of fibrofatty connective tissue, giving off infundibular branch(es) as it proceeds.
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Fig 5. The aorta and pulmonary trunk have been cut transversely across their sinotubular junctions, which are almost perpendicular, to show the relationships of the sinuses and the origin of the coronary arteries. Note how the zones of apposition of the facing arterial valvar leaflets meet at the level of the sinotubular junctions (star).
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Fig 6. The walls of the aorta have been cut away to reveal a fibrous band (arrow), which connects the top of the interleaflet triangle between the right and left coronary aortic sinuses with the top of the interleaflet triangle between the right and left facing pulmonary sinuses.
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Fig 7. This an enlargement of the dissection shown in Figure 4. The pulmonary root was removed by making a cut perpendicular to the attachment of the valvar leaflets throughout the root. Note that this cut has left a residual cuff of infundibular musculature, yet still permitted entire removal of the valvar leaflets. This would not be possible if a true muscular septum interposed between the pulmonary root and the left ventricle. The arrow shows the first septal perforating artery.
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In none of the infant hearts studies were we able to detect by gross dissection any discrete fibrous structures between the aortic and pulmonary roots. In 3 out of the 6 older hearts, in contrast, fibrous bands were easily demonstrable. The major band in each of these hearts joined the adventitia of the aorta at the top of the interleaflet triangle between the left and right coronary sinuses to that of the pulmonary trunk just to one side of the top of the interleaflet triangle between the right- and left-facing sinuses (Fig 6). The fibrous bands were short, and did not allow separation of the trunks by more than a few millimeters. They were relatively flimsy structures. In each of these hearts, additional thinner bands connected the great vessels in variable positions at or below the sinutubular junction. In none of these hearts was it possible to detect a fibrous raphe, or a remnant of such a raphe, within the long axis of the septal aspect of the free-standing infundibular musculature as had been illustrated by Mall [7].
Microscopic examinations
In the infant heart sectioned in the transverse plane of the aorta, a fine band of fibrous strands was found immediately below the level of the sinutubular junction. It extended between the adventitia covering the interleaflet triangle between the right and left coronary sinuses of the aorta and that covering the interleaflet triangle between the right- and left-facing sinuses of the pulmonary trunk. In the heart sectioned in the transverse plane of the pulmonary trunk, a dense region of fibers was seen occupying the same position between the sinuses. The collection of fibers was cut obliquely to the plane of section, and ran obliquely to the surrounding connective tissue fibers. No discrete longitudinal fibrous band was identified within the muscular wall of the free-standing subpulmonary infundibulum.
Studies in the operating room
A fibrous band, markedly tougher than the surrounding connective tissue, was noted to be present in half of the cases. It was located just below the sinotubular junctions, and connected the adventitia of the aorta at the top of the interleaflet triangle between the right and left coronary sinuses with that of the pulmonary trunk at the top of the interleaflet triangle between the right- and left-facing sinuses (Fig 8).
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Fig 8. A band of fibrous tissue as it is seen in the operating room, positioned between the tips of the blades of the scissors.
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Comment
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Our investigation, together with detailed analysis of the studies of the Leiden group [3, 5] has provided additional insights from our previous study [2] into the anatomic relationships between the aortic and pulmonary roots. These findings serve to clarify those controversies concerning the anatomic background to the Ross procedure which reflect differences in terminology as opposed to differences in observation. Crucial in this debate, nonetheless, is an understanding of what is meant by a "septum" [8]. This point is also surely of major significance to cardiothoracic surgeons, who must remove the pulmonary root from the heart using the safest technique so as to prepare it for use in the Ross procedure.
The dominant feature of the two arterial roots is their obliqueness relative to each other. The aortic root forms the keystone of the ventricular base [2, 3], whereas the pulmonary outflow tract spirals round the aortic sinuses. The aortic root cannot be removed in its entirety from the left ventricle without damaging the surrounding structures. In contrast, the leaflets of the pulmonary valve are lifted completely away from the base of the heart by the muscular free-standing subpulmonary infundibulum. It is this area that is removed in its entirety for use in the Ross procedure as the pulmonary autograft. Provided the removal is performed with care, and note is taken of the adjacent coronary arteries, and their branches, this procedure does not compromise the remaining ventricular structures. It is the very fact that the pulmonary valve is separated from the right ventricle and the base of the muscular ventricular septum by the free-standing subpulmonary infundibulum that makes possible the Ross procedure. By our understanding, a septal structure interposes directly between adjacent cavities of the heart [8]. Subsequent to our recent correspondence, the group from Leiden [5] maintained that a septal structure satisfying this definition separated the pulmonary root from the left ventricle in the region of the first septal perforating artery. Our further dissections show that this is not the case. Even in the region of the first septal perforating artery, it is possible to remove the infundibulum from the base of the right ventricle by making a cut perpendicular to the attachment of the pulmonary valvar leaflet (Fig 7). Our dissections do not substantiate the claim of Bartelings and colleagues [5] that such cuts would enter the cavity of the left ventricle. It is certainly safer to remove the pulmonary autograft using oblique dissection as demonstrated by Hokken and associates [3], but this should not obscure the anatomic fact that a sleeve of musculature raises the entire valvar structure away from the ventricular base.
Apart from this crucial difference, our findings are very much in accord with the observations of the Leiden group [5]. We agree with them that the musculature of the infundibulum is not rigid like the ventricular structures which support the aortic valve. Thus, subsequent to removal of the native valve, the anatomy allows a large, even adult-sized, pulmonary homograft to be accommodated even in an infant. We also agree with Hokken and colleagues [3] that it is important, in the Ross procedure, to trim back any muscle removed with the autograft so that it is used only as a sewing "ring," and not as a supporting structure for the neoaortic valve. The proximal end of the autograft must be seated such that the ventriculo-arterial junction of the autograft corresponds as closely as possible with that of the native aorta. In this way, the valve can be supported by appropriate structures. If this is done, dilation and subsequent incompetence of the new valve is very unusual. The tissues of the transposed pulmonary root are more elastic than those supporting a mechanical valve. It is this feature that make it possible to fit the pulmonary autograft into the aortic orifice without compromising the valvar mechanism, even though the two arterial roots are rarely of exactly the same diameter.
It is particularly important to appreciate the course of the proximal part of the first septal perforating artery so as safely to complete the Ross procedure. Septal infarcts were responsible for some mortality early in the use of this operation [9]. It is possible in many cases to remove the pulmonary autograft without visualizing the vessel. In some cases, however, because of the varying length of the free-standing muscular infundibular sleeve, the vessel is only a millimeter or so proximal to, or deep to, the hinge of the pulmonary valve. In these cases, again as emphasized by Hokken and associates [3], the musculature of the supporting right ventricular aspect of the septum should be sharply dissected obliquely along the plane created by the septal arterial branches. Some people talk of "2 layers" of the true muscular ventricular septum. Although in strict anatomical terms this is incorrect, the septal arteries lie in an oblique plane within the septum, such that a bevelled cuff of right ventricular musculature can be removed, by sharp dissection, together with the free-standing sleeve of the autograft. Failure to appreciate this point, and inappropriate use of transverse dissections, could lead, in some cases, to damage to the septal arteries. Thus, as noted by Bartelings and colleagues [5], the pulmonary autograft does, indeed, have a component that is seated upon the ventricular septum. This does not mean that this part of the infundibulum is a true anatomic septum. It is understanding the difference between the free-standing sleeve and the underlying septum which, for us at any rate, clarifies the anatomic arrangement.
Concerning tendons of the infundibulum, or their proxies, our findings are of more academic than practical significance. They serve, nonetheless, to clarify some ongoing controversies. Thus, our dissections in some hearts revealed a fibrous connection, of variable toughness, between the aorta and pulmonary trunk in the region of the intercoronary commissure. The fibrous band could be demonstrated microscopically in the hearts obtained from infants, but was too delicate to demonstrate by macroscopic dissection. We failed to demonstrate such a structure in half of the adult hearts, either because it was too fragile, or because it is not universally present. This tissue, which appears to acquire extra toughness in aging, may well be better developed in patients with aortic valvar disease than in the "normal" hearts examined here.
What, then, is the relationship of these fibrous connections demonstrated by us and the various ligamentous structures described by others? Barry and Patten [10] illustrated a "conus ligament" at approximately sinotubular level. They describe it as a "moderately distinct band of heavy fibers" joining the coronet-shaped "annuli" of the aorta and pulmonary trunks. Zimmerman and Bailey [11], in contrast, describe the "ligament of the conus," or "conus tendon," as connecting the pulmonary root to the rest of the fibrous skeleton. It was said to pass between the "left ascending limb of the right coronary cusp attachment" and the "apex of the nearest pulmonary subvalvar span." Their Figure 4, nonetheless, shows also a short and straight "tendon of Krehl" between "aortic annulus" and "pulmonic annulus." Their Figure 7, taken from Quain’s Anatomy [12] shows a long curved "conus tendon" running in the long axis of the subpulmonary infundibulum and curving around the aortic root. Their Figure 8 then shows a "conus tendon," described in the text as "ligament of the conus," which was said to pass from the sinotubular junction of the pulmonary trunk to the aortic root at the middle of the sinuses.
The figure taken from Quain’s Anatomy [12] is purported to reproduce the first figure from the study of Mall [7]. The figure of Mall, however, shows a short straight connection between the two roots. Mall states that this connection had been described well by Krehl in 1889, who interpreted it as the upper part of the "septum aorticum." The "tendon of the conus," according to Mall, gives rise to the muscle fibers that encircle the subpulmonary infundibulum. It is illustrated as being within the infundibulum, leading towards and blending with the "fila coronaria" (annulus) of the right atrioventricular junction. Here, therefore, we have an obvious conflict in Mall’s own writing. The tendon cannot, at the same time, be within the infundibulum and also at the sinotubular junction.
The fibrous structure that we have identified at the point of contact of the aortic and pulmonary roots is neither a tendon, nor is it related to the subpulmonary infundibulum. It cannot, therefore, be a "tendon of the infundibulum" as labeled by Hokken and colleagues [3], nor is it a long fibrous ligament as depicted by Zimmerman and Bailey [11]. It is simply a more densely fibrous area within the fibrous connective tissue binding together the two roots. This was the conclusion reached after our earlier study of this area [6]. Histologically, its fibers run in a different direction from those seen in the surrounding connective tissue. The surgical importance of the fibrous link is that, in many cases, the aorta and pulmonary trunk are closely adherent at this point. During dissection, care should be taken to keep close to the aorta, if necessary buttonholing it, to avoid inadvertently breaching the wall of the pulmonary autograft. This piece of fibrous tissue, of no clinical significance, can be divided with impunity. It is no more than an incidental finding encountered during dissection of the pulmonary autograft.
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Acknowledgments
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Professor Robert H. Anderson and Dr Siew Yen Ho are supported by the Joseph Levy Foundation and the British Heart Foundation. Professor Sir Magdi H. Yacoub is also supported by the British Heart Foundation.
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References
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Accepted for publication July 8, 1999.
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Abstract
Introduction
