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Ann Thorac Surg 2001;72:823-830
© 2001 The Society of Thoracic Surgeons
a Division of Pediatric Cardiovascular Surgery, University of Michigan School of Medicine, Ann Arbor, Michigan, USA
b Division of Pediatric Cardiology, University of Michigan School of Medicine, Ann Arbor, Michigan, USA
Address reprint requests to Dr Ohye, Division of Pediatric Cardiovascular Surgery, University of Michigan School of Medicine, F7830 Mott, 1500 E Medical Center Dr, Ann Arbor, MI 48109
e-mail: ohye{at}umich.edu
Presented at the Thirty-seventh Annual Meeting of The Society of Thoracic Surgeons, New Orleans, LA, Jan 29–31, 2001.
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Abstract |
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Methods. Between March 1993 and December 2000, 10 patients under 1 year of age underwent a Ross/Konno procedure at our institution (range, 2 to 349 days; median 16). All patients had severe to critical aortic stenosis. All patients required aortic annulus enlargement for size mismatch between the aortic and pulmonary valves.
Results. There were no deaths at a median follow-up of 48 months (range, 1 to 74 months). All patients had none to mild aortic stenosis on Doppler echocardiography. Eight patients had a 0 to 1+ aortic insufficiency, 1 patient had a 2+ aortic insufficiency, and 1 patient had a 3+ aortic insufficiency. Aortic annular dilatation was not observed. Aortic sinus dilatation occurred initially (mean change in z-value: 0 to 12 months, +2.1) and then stabilized (mean change in z-value: 12 to > 36 months, +0.6). No patient required additional procedures for aortic valve disease. Two patients required three pulmonary allograft replacements.
Conclusions. The Ross procedure with a modified Konno-type enlargement of the aortic annulus is an excellent approach to aortic valve disease in the neonate and infant. The procedure can be accomplished with low morbidity and mortality, and low rates of reoperation. The pulmonary autograft demonstrates durability without developing aortic stenosis, aortic insufficiency, or progressive dilatation. Enlargement of the aortic annulus parallels somatic growth.
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Introduction |
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There are also disadvantages to the Ross procedure. The harvesting of the pulmonary valve necessitates putting two valves at risk, for single valve disease. There have been a number of reports, predominantly in adults, describing dilatation of the aortic annulus, sinuses of Valsalva, and sinotubular junction after the Ross procedure [3, 4, 5, 6]. Some authors have reported that autograft dilatation is a significant cause of aortic insufficiency (AI) [3], while others have not seen the progression of AI despite dilatation [4, 5].
Data regarding patient and autograft outcomes in neonates and infants undergoing the Ross procedure are lacking [7]. In an effort to understand the utility of the Ross procedure in this population, we retrospectively reviewed the group of patients less than 1 year of age who underwent the Ross procedure at our institution. Major outcomes studied included patient survival, freedom from reoperation, aortic annulus dilatation, sinotubular junction dilatation, and aortic valve function.
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All patients underwent a Ross procedure utilizing the root replacement technique without wrapping either anastomosis. The pulmonary valve was harvested as previously published [7, 8] (Fig 1). Running polypropylene monofilament suture was used for both the proximal and distal anastomoses. Pulmonary homograft was preferentially used for pulmonary valve replacement when available in appropriate size. Seven patients received a pulmonary homograft ranging from 14 to 20 mm. One patient received a 19-mm pulmonary homograft downsized to 11 mm. One patient received a 15-mm aortic homograft and 1 patient received a 12-mm heterograft.
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Doppler/echocardiography
A single pediatric cardiologist reviewed all available follow-up echocardiograms. Measurements of the internal diameter at the level of the annulus and sinotubular junction were made perpendicular to the long axis of the aorta. Z-values for the sinotubular junction and aortic annulus were calculated using published standards [9]. Continuous-wave Doppler analysis was utilized to measure the maximum velocities across the aortic valve. Color-flow Doppler imaging was used to analyze the degree of AI. Insufficiency was graded from grade 0 (none) to grade 4 (severe) based on accepted criteria [10].
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The Ross procedure is also useful in the management of the difficult population of neonates with critical AS, and hypoplasia of the aortic annulus or left ventricular outflow tract, or both (ie, hypoplasia of the aortic annulus and left ventricular outflow tract). Removal of the diseased aortic valve and pulmonary autograft during the Ross procedure allows an unparalleled view of the left ventricular outflow tract and interventricular septum. This exposure facilitates the performance of either a modified Konno-type augmentation of the left ventricular outflow tract by dividing the aortic annulus and incising the septum, or a formal Konno septoplasty.
There are disadvantages of the Ross procedure as well. The nature of the operation places two valves at risk for single valve disease. In addition, there have been an increasing number of reports, predominantly in adults, describing dilatation of the aortic annulus, sinuses of Valsalva, and sinotubular junction after the Ross procedure [3, 4, 5, 6]. Some authors have reported that autograft dilatation is a significant cause of AI [3], while others have not seen the progression of AI despite dilatation [4, 5]. In those studies demonstrating progressive AI, the dilatation of the sinotubular junction, which distracts the leaflets preventing coaptation, is felt to be the primary pathology. As in patients with sinus of Valsalva aneurysms, dilatation of the sinuses itself does not lead to the development of AI [3, 6, 16].
Other disadvantages of the Ross procedure in adults are less applicable to the pediatric patient. The operation is technically more challenging than a straightforward aortic valve replacement. However, many pediatric patients are not candidates for a simple aortic valve replacement because of anatomic considerations and the lack of readily available, appropriately sized prostheses. Particularly in the growing pediatric patient, there is the need for pulmonary conduit replacement. Replacement of a pulmonary conduit is, however, less difficult than repeated aortic root replacement. Other concerns regarding the use of the Ross procedure in children include the uncertain long-term outcome of the pulmonary autograft in the aortic position.
Operative technique
The original descriptions of the Ross procedure involved the use of a subcoronary implantation technique [1]. However, technical difficulties with size mismatch and valve malposition led to an incidence of AI using this method [17]. This approach was subsequently abandoned in favor of the inclusion technique and the freestanding root replacement [8, 18]. Although data published on adult patients have shown an increased incidence of aortic sinus dilatation with root replacement when compared with the inclusion technique, root replacement remains the preferred approach of most surgeons [6, 12, 19, 20].
All patients in this study underwent a Ross procedure utilizing the root replacement technique. Other techniques in this population are not applicable. All patients in this study had severe to critical AS with associated hypoplasia of the aortic annulus and ascending aorta. With the exception of 1 patient who had previously undergone a Konno operation and aortic root replacement with an aortic homograft, all patients required enlargement of the aortic annulus. This was accomplished with a modified Konno technique. This approach consists of incising the septum, rather than completely dividing the muscle (Fig 2). A Morrow-type septal myomectomy may be added as necessary for subaortic obstruction. We have found it useful to anastomose the autograft to the endocardium of the right ventricular outflow tract in the area of the septal incision to ensure adequate strength of the suture line (Fig 2, inset).
Freedom from reoperation
The Ross procedure has demonstrated excellent rates of freedom from reoperation. Sir Donald Ross’ [2] series of adult patients have maintained an 85% freedom from reoperation for the autograft at 20 years. Of the patients requiring allograft replacement (n = 33), 19 were attributed to autograft malinsertion early in the experience. In the pediatric population, Elkins and colleagues [12] have reported a freedom from reoperation of 90 ± 4% at 8 years for the autograft, and 94 ± 3% for the homograft.
These results must be tempered for the very young patient, who is rapidly growing and has limited thoracic volume for the placement of a pulmonary homograft. In the current study, no patient required reintervention for aortic valve disease or recurrent left ventricular outflow tract. Overall actuarial freedom from reoperation and from conduit replacements was excellent. Choice of conduit appeared to impact the need for replacement. Of the 2 patients requiring RV-PA conduit replacement, 1 patient received an aortic homograft and the other patient received a downsized pulmonary homograft. Our preference has been to utilize an unaltered pulmonary homograft for RV-PA reconstruction whenever an appropriate size graft is available. In addition, we strive to place the largest conduit possible at the time of the Ross procedure. These data support this practice.
Other authors have found similar results for right ventricular outflow tract reconstruction. Tweddell and colleagues [21] reported factors adversely affecting homograft longevity to include the use of aortic homograft rather than pulmonary homograft and smaller homograft size. Homann and colleagues [22] demonstrated the superiority of homograft over xenograft in right ventricular outflow tract reconstruction.
The orthotopic position of the pulmonary allograft may also increase its longevity in comparison to other RV to PA conduits. Tweddell and colleagues [21] reported that an extracardiac operative technique was a risk factor for homograft failure in right ventricular outflow tract reconstruction. Laminar flow through a homograft in the pulmonary annulus may be less destructive to the valve than in situations where flow must change direction, as in a conduit sutured to the RV infundibulum. Heterotopic placement of the RV to PA conduit also potentially subjects the graft to compression by the sternum. In addition, conditions requiring heterotopic placement of the RV to PA conduit, such as pulmonary atresia, may have other distal pulmonary artery abnormalities impacting conduit performance.
Autograft annulus
While some studies in the adult literature have demonstrated dilatation of the autograft annulus after Ross procedure, most have not found annular dilatation to occur regardless of the implantation technique [5, 6, 19]. There are fewer studies of the fate of the autograft annulus in children. Elkins and colleagues [14] noted a significant increase in the z-value of the annulus of children when the root replacement technique was utilized, indicating dilatation. This was not the finding with the inclusion technique, in which annular diameter increased in concert with somatic growth. Solowiejczyk and colleagues [15] noted a similar finding in children, with a mean z-value change of +1.9 ± 2.4 at a median follow-up of 2 years when compared with normal values for the aortic valve. However, when normal values for the pulmonary valve were substituted, the changes in z-value were minimal (+0.7 ± 1.1), indicating change paralleling somatic growth. They also noted that while the autograft annuli were larger than normal aortic valves immediately after operations, they corresponded to normal pulmonary valve diameters.
In the present study, the mean autograft annulus z-value in the postoperative period was +2.1 ± 1.1. These z-values are based on the normal diameter for the aortic valve annulus. Thus, intuitively this result is not surprising because the pulmonary annulus is larger than the normal aortic annulus, and all patients underwent an enlargement of their aortic annulus to accommodate the autograft. Over the study period, the autograft annulus z-value remained stable. These data demonstrate that the change in the diameter of the autograft annulus parallels somatic growth. The slight negative trend in z-value suggests that perhaps the patients may be growing into their oversized aortic valves.
The differences between the current study and previous studies demonstrating autograft annular dilatation when compared with normal aortic valve diameters may be due to differences in the age distribution of the patient population. The median age in the present study was 16 days (range, 2 to 349 days), whereas the mean age in the study by Elkins and colleagues [14] was 11 years, and in the Solowiejczyk and colleagues [15] study, the mean age was 8.3 years. The procedure in which a similar age patient population had placements of the pulmonary valve in the systemic circulation is the arterial switch operation. Several studies have shown excellent intermediate and long-term performance of the neoaortic valve in this population. Serraf and colleagues [23] reviewed 753 patients who had undergone an arterial switch operation. Reoperation for aortic valve insufficiency was necessary in 3 patients. Similarly, Haas and colleagues [24] found only 3 of 285 patients required reoperation for aortic insufficiency after arterial switch operation. An explanation of the differences between neonates and infants, and older pediatric patients may be related to the fetal and postnatal development of the semilunar valves. The semilunar valves appear as endocardial covered mesenchymal tubercles from the truncus at approximately the sixth week of development. A study of the developmental changes of mucopolysaccharides and collagen in the murine semilunar valve by Colvee and Hurle [25] revealed that increases in chondroitin sulfate and decreases of hyaluronate continue well into the postnatal period. In humans, the pulmonary and aortic valves are structurally similar at birth, displaying further differentiation after birth, presumably caused by differences in pressure. (R. Anderson, personal communication, November 2000) Thus, the pulmonary valve in the neonate and infant may be inherently more plastic, allowing for differentiation into a more histologic aortic valve.
Nine of the patients underwent a modified Konno enlargement of the left ventricular outflow tract at the time of the Ross procedure. This modified Konno involved a simple incision of the annulus and septum without the insertion of a patch of prosthetic material. Without this supporting patch material, these patients would seem particularly at risk for annular dilatation. Again, the lack of annular dilatation may be caused by the inherent ability of the pulmonary valve of the neonate and infant to adapt to systemic pressure. In addition, Gorczynski and colleagues [26] found in vitro that the pulmonary valve annulus was less distensible than the aortic annulus, and that the tensile strength of the pulmonary valve leaflets were two to three times that of the aortic valve. These factors may all contribute to the lack of dilatation of the autograft annulus.
Autograft sinotubular junction
There have been a number of reports in adults describing dilatation of the aortic annulus, sinuses of Valsalva, and sinotubular junction after the Ross procedure [3, 4, 5, 6]. Some authors have reported that autograft dilatation is a significant cause of AI [3], whereas others have not seen the progression of AI despite dilatation [4, 5]. In the pediatric literature, there are fewer data, and no studies of a similar population of neonates and infants. In one of the few reports of pediatric patients, Elkins and colleagues [14] noted a significant yearly increase of aortic sinus z-value (+0.79 ± 0.19) in 14 patients who had undergone a Ross procedure by the root replacement technique in follow-up for a median of 27.5 months. A study of 40 pediatric patients in follow-up for a median of 2 years (range, 4.2 months to 5.4 years), Solowiejczyk and colleagues [15] found a mean sinus z-value increase of 1.3 ± 1.7. In the present study, the mean sinotubular junction z-value increased from 0 to 12 months, and then appeared to stabilize from 12 to greater than 36 months.
Again, differences in the median age of the study populations, 16 days in the current study, and 11 and 8.3 years in the studies by Elkins and colleagues [14] and Solowiejczyk and colleagues [15], respectively, may explain these discrepant results. As outlined above, the pulmonary valve of the neonate and infant may be better able to adapt to the pressures of the systemic circulation. The initial dilatation may represent stretch of the autograft, which occurs until the pulmonary autograft adapts to the higher pressure. Gorczynski and colleagues [26] demonstrated that the pulmonary artery at the level of the commissures is indeed more distensible than the aortic valve.
In particular, the neonatal pulmonary valve may be especially adept at rapidly adapting to the aortic position. Although all patient’s sinus z-values stabilized over the period from 12 to greater than 36 months, 4 patients demonstrated an increase of +3 or greater during the first 12 months. Of these 4 patients, 3 patients had their Ross procedure performed outside of the neonatal period. Furthermore, a total of 4 patients had their Ross procedure after the neonatal period, and of these 4, 3 patients had increases in their sinus z-values of +3 or greater in the initial 12 months. Of the remaining 6 patients who underwent a Ross procedure before 30 days of age, only 1 patient had a sinus z-value increase of greater than +2. The neonatal pulmonary valve may be uniquely able to handle the systemic pressures because of its exposure to high pressures in utero, as well as its ability to differentiate because of its immediate postnatal status.
Autograft function
No patient developed autograft stenosis or recurrent left ventricular outflow tract obstruction, and no patient required reintervention for autograft dysfunction. Eight patients had 0 to 1+ AI, 1 patient had 2+ AI, and 1 patient had 3+ AI. As expected, these 2 patients had the highest increases in sinotubular z-value (+3 and +4). In addition, both of these patients also underwent their Ross procedure outside of the neonatal period.
Overall, the performance of the autograft in the neonate and infant was excellent. Despite the technically demanding nature of the operation, the rates of survival were high and complications were low. These outcomes, combined with the low rates of reoperation, make the Ross/modified Konno procedure an excellent option for this difficult patient population. The autograft may be particularly appropriate for neonatal aortic valve replacement.
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Discussion |
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Your operative technique for aortic annulus enlargement is different than my own and what has previously been described by Hanley and others. We have made an incision across the annulus that is full thickness into the intraventricular septum, and we close this with a right ventricular free wall that is mobilized at the point we mobilize the pulmonary autograft. This avoids the use of a Dacron patch, and I think provides perhaps a better opportunity to enlarge the aortic annulus.
We have performed 176 Ross operations in children. These run from two days to seven years. We have had 11 patients who have required an aortoventriculoplasty, an additional 20 or so that have required a subvalvular resection and a left ventricular myomectomy, similar to what you have performed. Three of our eight deaths in the 176 patients were neonates that had required ECMO support prior or following a balloon valvuloplasty and were critically ill, I should say almost moribund, at the time we attempted the operation.
I raise the question, perhaps our results would have been improved in terms of survival if we had operated on these patients prior to their balloon valvuloplasty. Our actuarial survival in this group of patients at 12 years is 92%, and I provide the audience this information to allow them to put into perspective this small group of 10 patients. The actuarial freedom from autograft replacement is 94%, plus or minus 3%, at 12 years, and freedom from autograft degeneration, and if I can see the next slide, please.
This is our total experience in patients, and I apologize for not having this limited to children, but I only learned about discussing this early last week. But in our group of patients, we have 402 patients here, and you can see that the overall freedom at 10 years is 84% from autograft degeneration. In our pediatric population, our freedom from autograft degeneration is 90% at 4 years, and autograft degeneration includes autograft reoperation, valve-related death, or severe autograft insufficiency.
The actuarial freedom from homograft replacement in our pediatric age population is 90%, and I show this slide to show you that the blue line is our pediatric age population. Our freedom from homograft failure is 89% in 10 years in the total population, and it is 90% in the children. This actually underestimates the incidence of homograft dysfunction. A moderate number of these patients have some degree of homograft obstruction at this point and a small number have homograft insufficiency. This continues to remain as one of the Achilles heels for the Ross operation.
Since February of this past year, we initiated the use of a homograft valve which has had its HLA antigen markedly reduced. This has allowed us to implant a valve which does not produce HLA antibodies in its host. We hope this will significantly increase durability. At this point we have 49 patients who have been evaluated over a 3-month time period who have no evidence of the development of HLA antibodies in response to their grafts. I would ask Dr Ohye if they have considered the use of such a valve in his patients and what his feeling is about efforts to reduce the incidence of homograft failure.
I would say that we have been unable to demonstrate a difference between the autograft root replacement and the native pulmonary root following an arterial switch operation in terms of incidence of dilation. The degree of sinus dilation has been very similar in the two series of patients. Modulation of the autograft valve leaflet does occur after implant, and it has also been clearly demonstrated in numerous experimental studies. However, to date, we have seen no evidence of modulation of the pulmonary artery wall, and we have looked very carefully at all of our explant patients to try to demonstrate this. We have not had to explant an autograft valve in a neonate, so at this point we have no information about whether the neonate perhaps would modulate, but I am doubtful based on our’s and other studies.
I have enjoyed the presentation very much, it is a fine manuscript, your results in the neonatal period are excellent and bring into question the present enthusiasm for balloon valvuloplasty, especially in neonates with a small aortic annulus. I would ask you to say a few words about your decision-making process at your institution as to which neonate with critical aortic stenosis should have a balloon valvuloplasty and how you would get into the operating room with these patients for a Ross operation.
I would like to thank the Society for the privilege of the floor.
DR OHYE: I would like to thank Dr Elkins for his comments and acknowledge him as one of the champions of the Ross procedure in children upon which our data indirectly is based.
The first question was regarding the indications for the use of the Ross procedure versus balloon dilatation. Three of the patients in our study had undergone previous balloon valvulotomy; however, 2 of them were done at outside institutions. One of the criteria that we used to decide was obviously absolute aortic annulus size; for the average-sized neonate, 5 to 6 mm is one rough cut-off that we use. Some of these patients are not candidates for balloon dilatation because of other problems such as subaortic stenosis; 5 of our patients had significant subaortic stenosis, which obviously makes them not a candidate for balloon dilatation.
I would echo Dr Elkins’ comments about calling into question the use of balloon dilatation. Almost invariably the patients do have some degree of aortic insufficiency after their procedure. Also, in addition to leaving a volume overloaded ventricle, there is often a degree of residual aortic stenosis. Thus, the ventricle is also pressure overloaded, and whether or not in the long term this combination hurts the ventricle is the question. It has been our stance to be a little bit more aggressive about going straight to a Ross procedure than a balloon dilatation.
The other comments are in regard to particular homograft selection. We have not used any special homografts. It has been our practice to use pulmonary homografts. Of the two allografts that were replaced, one was an aortic homograft and one was a pulmonary homograft, which was downsized from 20 mm to 11 mm. So it has been our practice to use an appropriately-sized pulmonary homograft whenever possible.
Thank you.
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