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Ann Thorac Surg 2006;81:495-501
© 2006 The Society of Thoracic Surgeons

Original article: Cardiovascular

The Ross Procedure: New Insights Into the Surgical Anatomy

Horia Muresian, MD, PhD *

Cardiovascular Surgery, San Donato, and the Pathology Institute Niguarda, Milan, Italy

Accepted for publication July 18, 2005.

* Address correspondence to Dr Muresian, Cardiovascular Surgery, 36 Via Europa, 20097 San Donato, Milan, Italy (Email: cvsurg{at}hotmail.com).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: The precise knowledge of regional anatomical details is of utmost importance specially in complex procedures such as the Ross operation. This anatomical study offers a critical approach regarding the advantages, limits, and precautions for this procedure.

METHODS: Using dissection techniques, magnifications up to x6 and nontraditional approaches, 68 fixed normal heart specimens were studied over a 2-year period. The details of surgical relevance such as the boundaries and relations of the pulmonary and aortic roots, their vascularization, and the number and distribution of the septal arteries are described.

RESULTS: The aortic and pulmonary roots include interdependent elements functioning in a coordinated manner and establishing important relations with adjacent structures. Both coronary arteries vascularize the arterial roots. The infundibular branches from the right coronary artery are larger and more constant. The septal arteries establish important relations with the pulmonary infundibulum but their contribution to its vascularization is negligible. In this series, the main septal artery was the second, showing the longest retroinfundibular course. However, no constant relation was found between this vessel and the intraventricular landmarks.

CONCLUSIONS: A novel approach was used by performing nontraditional dissections of the arterial roots and by studying their vascularization The depicted details are useful to the surgeon specializing in the Ross procedure and represent the basis for further research.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Complex surgical interventions such as the Ross procedure [1] demand a periodical feedback with the continuously evolving anatomical knowledge. Good apprehension of the accurate anatomical details allows a better understanding of the requirements, facilitates the improvement of technical details, and avoids the potential errors and complications.

The Ross procedure [2] comprises the harvesting and preparation of the pulmonary autograft, its insertion in aortic position (utilizing the subcoronary, cylinder or root techniques), the reconstruction of the right ventricular outflow tract (RVOT), and depending on the technical variant, reimplantation of the coronary arteries, resizing (reduction or enlargement) of the basal ring or sinutubular junction, or both, and reinforcement of the neoaortic root. This is accomplished in successive steps both on beating heart and during the aortic cross-clamping period, with the aid of various techniques for myocardial protection.

Specific immediate complications of the Ross procedure [3, 4] are represented by bleeding, distortion of the coronary arteries, and injuries to the first septal artery, the left anterior descending artery (LAD), or the left coronary artery (LCA). Longer aortic cross-clamping time adds further deleterious effects.

Specific late complications include dilation of the neoaorta and aortic insufficiency [5–8], late-onset myocardial infarction [9], and degeneration of the homograft in pulmonary position [10, 11].

The aim of the present study was to identify and characterize the details of special surgical relevance for the Ross operation (and associated procedures).


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Fifty-six adult (age range, 25 to 81 years) and 12 pediatric (newborn to 14 years) normal hearts were studied at the Pathology Institute Niguarda, Milan, Italy over a 2-year period (2002 and 2003). Heart specimens were collected from patients of Caucasian descent with no cardiac or cardiovascular-related pathology (for example, stroke).

Hearts were harvested at autopsy. Buffered formalin (10%) was injected in the coronary tree antegrade and retrograde, reaching total volumes of 600 to 1,000 mL (depending on the size of the heart). Heart specimens were preserved in formalin for at least 3 weeks. Before dissection, specimens were immersed in ethanol (50%) for 30 minutes and rinsed in water. To reveal the arterial branches and their target tissues vascularized, veins were removed. Regular dissection techniques and magnifications up to x6 were employed, but nontraditional approaches were also used. (Not following the regular designs, dissections were planned and performed in order to expose the hidden details and intricate relations of the cardiac structures, specially those of surgical and echographical significance. See also Figures for details).

Photographic documentation was obtained with the aid of digital equipment (Olympus Camedia E-10; Olympus, Tokyo, Japan) and traditional equipment (Exacta; Zeiss Ihagee, Dresden, Germany [on Kodak 64T reversible color slide film]).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
The arterial roots function as the supporting structure of the aortic and pulmonary valves; they represent the origin of the respective vessels from their corresponding ventricle and include the distal ventricular outflow tract, the sinuses with the interleaflet triangles [12], and the sinotubular junction (Fig 1). The circle joining the bottom (nadir) of the valvar attachments, is the basal ring. The more distal circular anatomic ventriculoarterial junction is crossed by the crown-shaped insertion of the cusps; the latter extends between the basal ring and the sinotubular junction and constitutes the hemodynamic ventriculoarterial junction. These represent useful landmarks for diagnostic evaluation and surgery, as a true annulus does not actually exist [13].


Figure 1
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  		Fig 1. The aortic root, posterior view, of the adult heart. The tricuspid valve was retracted from the septum revealing the membranous septum (ms), which is continuous with the interleaflet triangle between the noncoronary sinus (NC) and the right coronary sinus (R). The mitral-aortic curtain is continuous with the triangle between the left coronary sinus (L) and the NC sinus. The levels of the basal ring (BR) and sinotubular junction (STJ) are marked with dotted lines. (Ao = aorta; RCA = right coronary artery.)

 
In the normal heart (Fig 2), the pulmonary cusps take off from a sleeve of free-standing musculature, and there is no obvious connection of the right ventriculoarterial junction to the fibrous skeleton of the heart. The tendon of infundibulum [14] (Fig 3) is at most a feeble structure, and it was present in only 2 of 68 specimens (2.94%).


Figure 2
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  		Fig 2. Adult heart dissected through the ventricular outflow tracts. Note the almost perpendicular disposition of the aortic and pulmonary roots, the general shape of the right ventricular outflow tract (RVOT) winding around the left ventricular outflow tract and the nonplanar disposition of the interventricular septum. The outlet septum corresponds to the dotted line. The RVOT is completely muscular whereas the posterior third of LVOT is formed by the anterior mitral leaflet (AML). The space between aorta (Ao) and pulmonary trunk (PT) lodges the left coronary artery (LCA ++ [here already bifurcated in the circumflex and left anterior descending arteries]). Note the close relationship between the Ao, PT, left atrial appendage (LAA), and LCA. The cleavage plane between the two roots is evident distally, while proximally, it becomes less distinct. Note also the thinner and shorter posterior wall of the autograft. (A = anterior tricuspid leaflet; CS = crista supraventricularis; L = left coronary sinus; NC = noncoronary sinus; P = posterior tricuspid leaflet; R = right coronary sinus; S = septal tricuspid leaflet; TM = tricuspid medial papillary muscle.)

 

Figure 3
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  		Fig 3. Left-basal view of the adult heart. The pulmonary trunk (PT) is retracted in order to expose the infundibular arteries (*) and the cleavage plane between the arterial trunks. In this specimen, a tendon of infundibulum is readily visible (x). The left atrial appendage (LAA) is also retracted to demonstrate the origin of the left coronary artery (LCA), of the circumflex branch (Cx), and of the left atrial branch (LAB). Note also the double origin of the sinus node artery and the retroaortic anastomotic circle between the LAB and right atrial branches (RAB). The right infundibular arteries are more conspicuous and have origin in an accessory right coronary. The posterior left infundibular artery originates proximal to S1; the lateral left artery, between the S1 and S2. Note also the large caliber of the S2 in this case. A branch (<<) from the RAB is given to the aortic root. (Ao = aorta; D1, D2 = diagonal branches; LAD = left anterior descending artery; RAA = right atrial appendage; RCA = right coronary artery; S1, S2, S3 = anterior septal arteries.)

 
Wedged between the remainder cardiac structures, the aortic root [15] was centrally located. About two thirds of its circumference was formed by ventricular (septal) myocardium; while roughly one third was fibrous, corresponding to the anterior mitral leaflet (mitral-aortic curtain) and to the two fibrous trigones (Fig 2).

The two roots cross each other at almost right angle; the distal part of the septum (outlet septum) corresponds to the interleaflet triangle between the left and right aortic sinuses, and on the pulmonary side, to the space between the two limbs of the trabecula septomarginalis. The trabecula septomarginalis showed in this series a high degree of variability regarding its width, distance from the pulmonary valve, and the anterior limb. In 8 specimens (11.76%), it was barely visible.

The main relations of the arterial roots are presented in Figures 2 through 4. Go The arteries ending in the septum having diameters of greater than 1 mm in the adult group and greater than 0.5 mm in the pediatric group were identified as septal arteries. The main septal artery was defined as the largest and longest artery in the given specimen.


Figure 4
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  		Fig 4. Infundibular vessels after autograft excision of the adult heart. The anterior septal artery S1 has a very proximal origin (and remote from the infundibulum); S2 is the largest. A cleavage plane exists between the muscular layers of the septum. There are three right infundibular arteries originating in an accessory right coronary and only one on the left (cut). Note also the position of the anterior septal arteries S1, S2, and S3 with respect to the infundibulum. The main septal artery, when not the first, shows a longer retroinfundibular course. (Ao = aorta; Cx = circumflex branch; LAD = left anterior descending artery; LCA = left coronary artery; RCA = right coronary artery.)

 
The septal arteries traveled between the right and left margins of the septum, at varying depths but never subendocardially. No correlation could be established between the location of the main septal artery and intraventricular landmarks: trabecula septomarginalis, crista supraventricularis, and tricuspid medial papillary muscle.

The characteristics of the septal arteries are presented in Table 1. Most frequently in this series, the main septal artery was the second septal artery originating left of the infundibulum and having the longest retroinfundibular course. In specimens with a clearly identifiable trabecula septomarginalis, 1 or 2 arterial branches traveled close to this landmark but their caliber, origin, and proximal course were highly variable [16].


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  		Table 1. Characteristics of the Anterior Septal Arteries
 
The pulmonary infundibulum is vascularized by branches from both coronary arteries [17] (Table 2, Figs 3 and 4). The most constant and conspicuous branches were given by the RCA or its accessory branch. Infundibular branches were named right or left following their origin from the right coronary sinus or RCA, left coronary sinus or LCA, respectively. Posterior infundibular branches vascularized the adjacent aspects of the arterial roots while the anterior, the infundibular free wall.


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  		Table 2. Characteristics of the Infundibular Arteries
 
Different from other series, only the branches from the right coronary sinus vascularizing most of the right ventricle (through infundibular, anterior and right marginal branches) were counted as third coronary arteries and were present in 3 adult and 1 pediatric specimens (5.88%).

The septal arteries did not contribute to the vascularization of the infundibulum. Instead, these vessels vascularized the tricuspid medial papillary muscle, the trabecula septomarginalis (proceeding into the moderator band) and the aortic root anastomozing with the atrioventricular node artery (Figs 5 and 6). The branches vascularizing these regions did not always have origin in the same septal artery.


Figure 5
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  		Fig 5. Interventricular septum and aortic root of an adult heart. The infundibulum was removed. The right ventricle cavity is widely open. The aortic sinuses were excised, revealing the interleaflet triangles. The coronary buttons are still attached to the aorta by a rim of tissue. The aortic root, corresponding to the space between the left coronary sinus (L) and right coronary sinus (R), and to the outlet septum, is vascularized by two early septal branches with origin in the proximal left anterior descending artery (LAD). In this specimen, S3 is the largest. Note its branches to the aortic root, to the tricuspid medial papillary muscle (TM), and the trabecula septomarginalis. A left infundibular artery (*) is visible, with origin between S3 and S4. (A = anterior tricuspid leaflet; Cx = circumflex branch; D1, D2 = diagonal branches; LCA = left coronary artery; P = posterior tricuspid leaflet; RCA = right coronary artery; S = septal tricuspid leaflet; S1, S2, S3, S4 = anterior septal arteries.

 
The aortic root is well vascularized (Table 3). The vessels for the distal muscular LVOT are the anterior and posterior septal arteries and the atrioventricular node artery [18].


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  		Table 3. Vascularization of the Aortic Root
 
The aortic sinuses receive collaterals from the main trunks or from their atrial [19, 20] or infundibular branches (Fig 3).

No coronary artery variation was found in this series.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
The elements composing the pulmonary root, function in a coordinated manner. Their structural relations and functional characteristics must be maintained even when working in the new aortic milieu under higher pressure regimens.

The actual location and extension of the pulmonary sinuses might not be readily apparent from the outside. Autograft harvesting usually starts with a distal incision at the level the pulmonary trunk, the valve can be checked if suitable for the procedure, and the proximal limit of the autograft is defined by passing a right-angled clamp across the valve.

The crista supraventricularis marks the proximal limit of the infundibulum [21] corresponding to the ventriculoinfundibular fold (as the right ventricle winds around the left); consequently, the anterior wall of the infundibulum has a larger extent. allowing to tailor a wedge-shaped muscular patch when a septoplasty in envisaged.

Owing to the lack of an annulus, because of its thinner and weaker walls, the pulmonary autograft can be easily distorted. Stay sutures (under the interleaflet triangles) or loading the graft on a Hegar probe can aid in handling, sizing, preparing, and inserting the autograft in aortic position. Autograft reinforcement (wrapping with synthetic patch or pericardium) is frequently employed in the root technique to prevent dilation and neoaortic insufficiency, but this may interfere with its normal function and growth.

Matching the size and length of the autograft to the aorta represents an essential step of the Ross procedure. The diameter of the distal anastomosis (sinotubular junction level) should be smaller than the proximal (basal ring level) [22]. The distal anastomosis of the autograft should be performed just distal to the sinotubular junction of the appropriately plicated native aorta to prevent dilation at this level. An ideal basal ring to sinotubular junction ratio of 1.1 for the neoaorta was experimentally found [23]. The muscle cuff of the autograft (basal ring level) should be as short as possible, about 4 mm [24].

In humans, the aortic sinuses have a normal asymmetry (probably of hemodynamic significance): right coronary sinus greater than noncoronary sinus greater than left coronary sinus. An aortic tilt angle (5.47 degrees) between the planes of the basal ring and of the sinotubular junction results [25].

Differences in the asymmetrical expansion of the aortic and pulmonary roots should also be considered for the implantation of the pulmonary autograft in the most physiological position. The expansion in the aortic root is as follows: right greater than left greater than noncoronary sinus; in the pulmonary root: right greater than anterior greater than left [26]. Morbid changes or anatomic variations of the aortic valve can pose special problems in adapting the autograft in aortic position.

The right and left infundibular arteries form peri-infundibular intercoronary anastomotic circles; they represent a potential source of bleeding with autograft harvesting and become conspicuous in coronary disease [27]. Moreover, branches from the RCA vascularize both arterial roots. Dissection of the infundibulum should proceed laterally (right and left) with the cautery and best on beating heart. Large right infundibular arteries may require surgical ligature. The arteries to the aortic root can easily bleed with extensive dissection and may resemble an anastomotic leak, especially when dissection was carried out with the aorta cross-clamped.

The loss of vascularity of the pulmonary autograft, working at higher intraluminal pressures, may contribute to its aneurysmal dilation after the Ross procedure and might impede its active growth. Microscopic examination of explanted autografts could offer an answer in the future.

The number of anterior septal arteries in this series, although greater than in some recent studies [28], was congruous with the corrosion cast technique [18]. The main septal artery was the second: differences between authors probably reflect the very definition of a septal perforator (position, target tissue, origin, caliber). Some of the early septal branches from the LAD did in fact vascularize the outlet septum and were found even in the juxtainfundibular area (proximal to the perpendicular line joining the tricuspid medial papillary muscle to the diaphragamtic surface of the heart) [28] (Fig 5). The main septal artery vascularizes a large area of the muscular septum and anastomoses with the atrioventricular node artery; ventricular dysfunction, arrhrythmias, and sudden death may be a consequence of the damage to this vessel [28].

Incisions through the fibrous part of the LVOT (Nicks and coworkers [29] and Manouguian and Kirchhoff [30]) have little effect on the vascularization of the aortic root but allow limited enlargements. Aortoventriculoplasty (Ross-Konno procedure) [31] will interrupt one or more septal arteries but consequences are still difficult to predict in the individual patient.

Coronary angiogram is not routinely performed in view of the Ross procedure if not otherwise specially indicated, but when such data become available, a careful review may aid the surgeon in identifying the main arteries and outline their reciprocal relations (between the septal and diagonal branches) or the presence of any coronary variation that might preclude autograft harvesting [32]: origin of the LAD from the RCA or right coronary sinus and preinfundibular course or anomalous origin of the LCA with retroinfundibular course (single coronary type II).

Although impaired coronary flow reserve was not demonstrated after the Ross procedure [33], reimplantation of the coronary buttons must be accurately done. Coronary mobilization is performed before their reimplantation. The use of large buttons is recommended in order to avoid anastomotic complications [34]. Substantial manipulation and careful repositioning is sometimes necessary in cases with bicuspid aortic valve and opposite coronary ostia. The proximal branches of the coronary arteries can limit their mobilization and may facilitate angulation and distortion of the main trunks if extensively pulled. The coronary buttons can be kept connected inferiorly to the aorta by preserving a small bridge of tissue that can be cut just before completing the reimplantation (Fig 5). The ostium of conspicuous third coronary arteries (as defined in this series) should be included in the RCA button owing to their importance in the vascularization of the right ventricle.

Injury to the septal arteries can be avoided by performing a superficial dissection of the posterior wall of the infundibulum. Injury to the LCA and LAD, especially in difficult redo operations, can be avoided by catheterizing the vessels with a coronary probe (but this requires dissection with the clamped aorta).

Macroscopically, three layers of the muscular interventricular septum can be distinguished, the rightmost of which can be sometimes peeled off the left ones, allowing a safer harvesting of the pulmonary autograft and exposing the septal arteries (Figs 5 and 6). Beyond the tricuspid medial papillary muscle and toward the apex, these layers become less distinct as the angle of intrusion of the wedge-shaped myocardial functional units changes [35]. Such a cleavage plane appears to be produced by the very passage of the septal arteries and not by a folding ventricular myocardial band [36].

Conclusions
Although this study demonstrated hitherto undescribed anatomy of the arterial roots and their arterialization, a correspondence with data in the living patient is required.

The functional structures of the arterial roots are complex and can be altered at various levels by the pathological states; even more, the circumventing arteries show particular patterns of distribution. All these details should be considered by the surgeon while contemplating such a complex procedure. The study revealed no absolute safe landmarks to avoid vascular complications. The surgeon equipped with important details should be able to anticipate, recognize and correct any unfavorable event. Still, other factors render some surgeons apprehensive about doing the Ross operation, for example, turning a one-valve disease into a two-valve disease, the problem of progressive neoaortic insufficiency, the need for conduit exchange, and the unclear use of the procedure in patients with bicuspid aortic valve disease. These concerns need to be addressed in the future.


Figure 6
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  		Fig 6. Vascularization of the aortic root of the adult heart. In a more advanced dissection of the aortic root, the tricuspid medial papillary muscle (TM) was retracted. The branches to the aortic root given by S1 (<<) are large and travel toward the membranous septum (dotted line) where they anastomose with the atrioventricular node artery (AVNA) and with the posterior septal artery branches (p [from the right coronary artery in this case]). (LAD = left anterior descending artery; LCA = left coronary artery; p = posterior septal arteries; S1, S2 = anterior septal arteries.)

 

   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
The author wishes to thank Dr Kunwar P. Bhatnagar, Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, Kentucky, USA, for the critical review of the manuscript.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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Further Anatomical Insights Regarding the Ross Procedure
Ann. Thorac. Surg., February 1, 2006; 81(2): 411 - 412.
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