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Ann Thorac Surg 2006;82:940-947
© 2006 The Society of Thoracic Surgeons
Center of Congenital Cardiac Disease—Sana Cardiac Surgical Clinic Stuttgart and Paediatric Cardiac Unit Olgahospital, Stuttgart, Germany
Accepted for publication April 24, 2006.
* Address correspondence to Dr Böhm, MD, Sana Herzchirurgische Klinik Stuttgart, Herdweg 2, D-70174 Stuttgart, Germany (Email: joboehm{at}z.zgs.de).
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Abstract |
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METHODS: Of 404 Ross operations done before November 2004, 60 were young patients with a median age of 12 years (range, 1 to 20 years). The pulmonary autograft technique universally was as a free root. A cryopreserved pulmonary homograft reconstructed the right ventricular outflow tract.
RESULTS: Early postoperative complications were reentry for bleeding in 2 patients and one pacemaker insertion. No thromboembolic or hemorrhagic events occurred during the follow-up of 42 ± 27 months. Two late deaths occurred, one from myocardial infarction after 3 months and another sudden death after 5 years, probably from critical pulmonary homograft stenosis. Echocardiographic follow-up revealed a median peak gradient of 6.3 ± 3 mm Hg across the autograft. The median pulmonary homograft peak gradient of 19.1 ± 13.7 mm Hg was increased to more than 30 mm Hg in 6 patients. Another 6 patients had moderate but clinically insignificant pulmonary homograft regurgitation. Altogether, 6 patients required reoperation for replacement of stenotic homografts. No autograft related reoperation occurred.
CONCLUSIONS: Young patients with the Ross operation had good mid-term autograft function and no perioperative mortality. Factors that justify the choice of the Ross operation for young patients are the normal physiologic hemodynamics and growth of the autograft as well as freedom from anticoagulation. A 10% reoperation rate, elevated pulmonary homograft gradients, and the surgical complexity remain limiting factors.
Aortic valve replacement and prostheses choice for children is more challenging than in adults. The problems of patient-prostheses mismatch, growth of the child, and anticoagulation all contribute to the complexity of the problem. Despite the variety in designs of conventional mechanical and biologic valve prostheses, the available prostheses and developments are still far from ideal [1]. The ideal valve prosthesis in children should offer appropriate hemodynamics even in small sizes, avoid anticoagulation, which is fraught with complications in young children, and should also potentially grow with the child. Freedom from anticoagulation allows unrestrained activity and thereby normal psychosocial development of the growing child. Female patients should avoid systemic anticoagulation during pregnancy. Particularly small prostheses that do not grow with the child eventually become obstructive and require replacement.
The pulmonary autograft, or Ross operation, as an aortic valve replacement potentially provides the solution to most of these problems, albeit at the cost of a double valve procedure in which one of the valves replaced, the pulmonary valve, is healthy and for which in children, particularly, ideal replacement devices do not exist. After the first pulmonary autograft operation by Donald Ross in 1967 [2], this technique of aortic valve replacement has been reproduced safely by others and gradually received increasing recognition from both pediatric cardiologists and cardiac surgeons [3]. Experience with the Ross operation at our unit dates from 1995, and initially only adult patients were considered. The initial results led us to include children in the program beginning in July 1996 [4]. In this study, we review the results in all 60 children and adolescents who received the Ross operation.
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Patients and Methods |
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Mild hypothermic extracorporal circulation was used in all patients (33°C to 36°C), and intermittent antegrade and retrograde cold blood cardioplegia was chosen for myocardial protection. A brief description of the technical aspects of the surgical procedure in children follows.
Excess muscle skirt on the autograft was not used to compensate for size discrepancy between the autograft and the aortic annulus because excess muscle in the free root-replacement technique has been implicated in subsequent autograft dilatation and incompetence. In cases of mismatch, reduction of the aortic annulus was achieved by commissural plication. Enlargement was achieved by classical incision through the aortic annulus into the anterior leaflet of the mitral valve. In the latter case, the autograft was sutured directly to the incised tissue and no interpositioning of patch material or other tissue was used. If the left atrium was entered, it was closed with direct suture.
After we had observed subsequent recurrent annular dilation in the occasional adult patient after annular plication for geometric mismatch, we subsequently routinely buttressed the aortic annulus with a complete circumferential external strip of Dacron (DuPont, Wilmington, DE) or Hemashield (Boston Scientific Corp, Natick, MA) whenever the annulus was plicated for mismatch [4]. In children, however, we had to allow for autograft growth, and external buttressing was not always included. In case of substantial remodeling of the aortic annulus, only the area of plication was supported. A strip of autologous untreated pericardium was used instead of rigid synthetic fabric.
In our adult patients with aortic ectasia and autograft mismatch, we regularly replace the ascending aorta with graft prostheses from the sinotubular junction, thereby stabilizing the sinotubular junction. The ascending aorta is only replaced in children if adult dimensions are attainable, and a remodeling with wedge resection of the aortic wall to the ideal sino-tubular size was generally preferred. In children, the RVOT was replaced with an adult size homograft whenever possible, as homograft size is implicated strongly in homograft durability [6]. All operative data and concomitant procedures are listed in Table 2.
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All data were expressed as mean ± standard deviation unless otherwise indicated. Time-to-event analysis for homograft function was performed by Kaplan-Meier estimation with use of the statistical software SAS 9.1.2 (SAS Institute, Cary, NC). For comparison of independent groups of continuous or binary data, the two-sample t test and the Fisher exact test were used, respectively. For all tests, p < 0.05 was considered significant.
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Results |
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There was no operative or early mortality. All early morbid events are listed in Table 3. No thromboembolic or hemorrhagic events or endocarditis were observed (Table 4). One 11-year-old girl died shortly after 3 months from an anterior myocardial infarction, confirmed at autopsy. At the time of the Ross operation, weaning from cardiopulmonary bypass was only possible after performing a single coronary artery bypass grafting to the proximal right coronary artery. This was done for suspected right ventricular ischemia owing to suspected malposition of the extremely small right coronary artery, reinserted as a button. Her subsequent postoperative course was uneventful, and she recovered completely. No right ventricular infarction was found at autopsy, and the graft and native vessel were patent to the right. The etiology of the documented left ventricular anterior myocardial infarction remained unclear.
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No reoperations have been done because of autograft malfunction, and no reoperations are pending in this series of young patients.
A rapid, progressive homograft stenosis in one 8-year-old boy led to reoperation for pulmonary homograft replacement 8 months after the Ross operation, as published recently [5]. This patient had received a previous aortic homograft as an aortic valve replacement before the Ross operation. The homograft conduit was symmetrically narrowed throughout its length and was obviously fibrotic. It was widened with a synthetic Dacron patch at the first reoperation. The gradient improved but recurred after 4 years despite attempts at balloon dilation, and he was referred back for homograft replacement. The pulmonary homograft was then replaced with a commercially manufactured decellularized homograft (Cryolife Inc, Kennesaw, GA).
Balloon valvuloplasty was attempted in 3 patients but was universally ineffective, and any palliation of homograft stenosis that was achieved lasted only a few months. Balloon dilatation of pulmonary homograft stenosis was subsequently abandoned in favor of frequent echocardiographic observation combined with magnet resonance imaging. Homograft replacement was suggested earlier and from a gradient of 50 mm Hg or more, or alternatively, as soon as signs of right ventricular overload become apparent.
To date, 6 patients required pulmonary homograft re-replacements, and in most patients, severe proximal stenosis and fibrosis were the indication for reoperation. Data of the homografts explanted are listed in Table 5. A further 6 patients have been documented to have an echocardiograph gradient across the RVOT of greater than 30 mm Hg at the latest follow-up and are under close clinical observation pending surgery. Freedom from homograft reoperation or a gradient of less than 30 mm Hg was estimated at only 64% (standard error, 0.09) 72 months after the Ross operation (Fig 2). The echocardiographic results are presented in Table 6.
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Comment |
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Several groups have documented the superior hemodynamic performance of the pulmonary autograft [9–11]. This performance is also superior to that of the aortic homograft [12]. These hemodynamic properties and the impressing reverse-remodeling of left ventricular dimensions contribute to the quality of life achieved in most patients after the Ross operation, an observation reported by several groups [12–14]. The zero hospital mortality is gratifyingly low for our series compared with other series with the Ross operation in children: The experienced groups of both Elkins and colleagues [15] and Pessotto and colleagues [16] reported an early mortality of 3.5% and 2.7%, respectively.
A comparison with a patient group of similar age and number treated with conventional mechanical prostheses is difficult, and the number of children treated with alternative prostheses at our unit is too small to enable a statistical comparison. Our own institutional experience with such young patients treated with homograft or mechanical aortic valve replacement in the same time period from 1995 until 2004 consists of 15 patients. A documented decision against the Ross procedure in these patients was made due to active rheumatic fever in 3, Marfan syndrome in 2, extreme aortic annulus dilatation, hypoplastic pulmonary root, earlier mechanical prosthesis in mitral position and personal preference for a homograft implantation in active endocarditis and drug abuse in one case each. Referring physician preference was the probable reason for alternative prostheses in the remaining patients.
In 7 of these patients who received mechanical prosthesis, valve re-replacement due to pannus ingrowth, and another near fatal valve thrombosis occurred in one case each. As far as could be determined, minor hemorrhagic events occurred in 2 patients. Of the 8 patients who received an aortic homograft, 1 died early postoperatively from a myocardial infarction, degeneration led to homograft re-replacement in another patient, and a further 2 patients are known to have either moderate homograft stenosis or a combined stenotic and incompetent valve dysfunction. No special efforts to document the clinical course of these patients were made, in contrast to the Ross operation group, and it is possible that the retrospective nature of the information regarding valve related complications although already high, has led to under-reporting.
Alexiou and colleagues [17] described their clinical results in a group of 56 children who received conventional mechanical prostheses. They reported both an operative mortality of 5.4% (3/56) and complete heart block in the same number of patients, and other significant valve-related complications occurred in 14.3% (8/56). Compared with the Ross series of the current report, the Alexiou group's series of children with mechanical prostheses were younger (11.2 years versus 12.6 years), more frequently in New York Heart Association (NYHA) functional class III to IV (50% versus 22%), required multiple cardiac surgical procedures more frequently (64% versus 47%), and therefore, represent a group with more complex pathology, which could explain their higher perioperative mortality and morbidity. Conversely, 24 of these 48 concomitant surgical procedures were for aortic root enlargement, which is considered an inherent part of prosthetic valve surgery in growing children with small aortic roots. Only 3 of our Ross patients (5%) required root enlargement, despite which no patients had significantly elevated gradients across the left ventricular outflow tract (LVOT).
The coronary artery bypass required in 1 patient of our series was unfortunate and does reflect the complexity of the Ross procedure, particularly in patients with concomitant congenital abnormalities. Coronary artery occlusion, though, is not absent from other studies of aortic valve prosthetic surgery both in adults as well as in children, as described by Alexiou and colleagues [17].
A more direct comparison is provided by Lupinetti and colleagues [18], who reported a nonrandomized but comparable group of 26 pediatric patients who received mechanical prostheses with another group of 25 patients of similar age and who underwent either the Ross operation (n = 19) or who received an aortic homograft (n = 6) where the Ross operation was contraindicated because of connective tissue disease. Operative complications included two mild strokes and one pacemaker in the autograft/homograft group compared with three deaths and two pacemakers in the mechanical prostheses group. Event-free survival at 2 years was comparatively low, with 67% for the mechanical group in contrast to 96% for the autograft/homograft group. Reoperation-free survival of 96% at 2 years again was also superior for the autograft/allograft group compared with the somewhat disappointing 80% of the group treated with a mechanical valve replacement. One Ross operation recipient required reoperation for pulmonary homograft stenosis, and the mechanical prostheses group required three reoperations for subvalvar pannus formation, endocarditis, and paravalvular leakage.
In the present Ross recipient study, the freedom from anticoagulation and freedom from frequent blood testing together with a complete absence of thromboembolic or hemorrhagic complications contributed to quality of life and the possibility of a normal childhood, advantages that are not possible with mechanical prostheses. Two of our female patients, who received the Ross operation as adolescents, later decided to have families, and for both, the pregnancy and childbirth were completely uneventful and routine. Thus, the Ross operation offers a striking advantage compared with mechanical valve prostheses for young female patients. A report from Dore and Somerville [19] of 14 pregnancies in 8 young women after pulmonary autograft valve replacement, without valve-related complications, supports this observation.
The use of conventional biologic prostheses in children avoids anticoagulation, but their general use is limited owing to the disappointing durability of biologic valve tissue, especially in children [20, 21]. Aortic valve replacement with the use of cryopreserved aortic homografts has, unfortunately, not proven to be a convincing alternative in these young patients. O'Brien and co-workers [22] reported an unacceptably low freedom from structural deterioration at 10 years of only 43% ± 22% for patients up to 20 years of age, significantly worse than in adult patients.
Fortunately in our series, no autograft failure or autograft-related reoperation has occurred in these younger patients in up to 84 months of follow-up. In contrast to our results, Elkins and colleagues [23] reported an autograft-related reoperation rate in their pediatric patients of 6.2% (11/178) after 12 years, mainly owing to autograft valve regurgitation.
The series reported from Laudito and colleagues [24] reveals a surprisingly higher autograft failure rate of 9.7% (7/72) during a follow-up period of up to 80 months. The reasons for this higher failure in their series are not evident. Possible reasons might be the very young age of their patients (median age, 9.1 years, 81% <15 years old) and their failure to reduce or at least partially fix the aortic annulus in these patients, presumably owing to concerns about future growth. Accompanying vascular particularities of patients with congenital aortic valve malformations may be of relevance as mentioned in several other reports [25, 26].
Somatic autograft growth is well recognized, and the advantages of this have been verified by clinical observation [15, 27] and animal experiments [28]. When the autograft is inserted in a free-root replacement technique, passive dilatation and somatic growth occurs [27]. According to data of Elkins and colleagues [15], passive dilatation seems to be of lesser importance with the root inclusion technique.
The aortic annulus diameters of our patients standardized to the patients' body surface area and expressed as the number of standard deviations from the mean value of a normal population (z value, normal deviation; Human Heart Valve Chart, CryoLife Inc, 1999) indicate an enlarged annulus with a z value of 1.66 ± 1.7 compared with the expected diameter of normal aortic valves, but when otherwise compared with the diameters of pulmonary valves of the same normal population, the z value of 0.02 ± 1.4 reveals little difference. Calculating z values with the use of normal dimensions derived from autopsy studies might be questionable, however, especially when echocardiograph data were compared during follow-up.
The regression equation introduced by Daubeney and colleagues [29] based on the normal dimensions derived from two-dimensional echocardiography might, therefore, be more representative to calculate z values.
For our patient-group, we calculated a z value of 1.01 ± 2 for the autograft regarded as an aortic valve and for comparison –0.32 ± 1.2 as an original pulmonary valve, which confirmed the above observation. This is also in accordance with data from Pessotto and colleagues, who recently reported similar results in their pediatric population treated with the Ross procedure. They concluded that the pulmonary autograft continues to grow as a normal pulmonary root, even when placed in the aortic position [16]. We therefore conclude that our policy of partial buttressing of only the tailored portion of the aortic annulus, where plication was necessary during the Ross operation, did prevent undue annular dilatation and also allowed appropriate somatic growth of the pulmonary autograft.
The sinus of Valsalva dimensions could be recorded over time in a reliable manner in 33 of our patients. Sinus dilation of the autograft to more than 42 mm in diameter occurred in 9% (3/33). Simon-Kupilik and colleagues [30] reported a similar autograft sinus dilatation in 7% of their adult patients that were also all performed as free root replacements, and they considered an autograft sinus diameter of more than 37 mm as root dilatation, a threshold crossed by 52% of their patients after 60 months of follow-up. In our series, 45% of the pediatric patients (15/33) also exceeded this limit. Comparison of our series with the series of Simon-Kupilik and colleagues might be difficult owing to differences in patient ages and length of follow-up.
With respect to published data of Hokken and colleagues [31], about 40% of this increase in sinus diameter appeared 7 to 10 days after the Ross operation and was observed to be most prominent during the first postoperative year. Thus, differences in length of follow-up might be of minor importance, and we assume that autograft dilatation in pediatric patients after the Ross procedure resembles autograft dilatation in adult patients.
The 15 patients from our series with a sinus diameter exceeding 37 mm also presented with a significantly greater aortic annulus at follow-up, with a mean diameter of 26 ± 2.8 mm compared with 20.6 ± 2.6 of the other 18 patients with a sinus dimensions of less than 37 mm (p < 0.0001). This implies dilatation of the entire autograft conduit at all levels. None of the patients with a sinus diameter exceeding 37 mm had required aortic root enlargement at time of the Ross operation. These findings imply an intrinsic tissue abnormality of the pulmonary root in those patients with congenital aortic valve disease, as has been proposed by others [25, 26]. Of interest is that patients from the group with a sinus diameter exceeding 37 mm more frequently required annular plication at the Ross operation (7/15 versus 4/18) and also presented more frequently with aortic insufficiency as the primary pathology as indication for aortic valve replacement (6/15 versus 3/18), but without statistical significance (p = 0.16 and 0.24, respectively).
Autograft dilatation at the level of the sinuses of Valsalva has been confirmed by several groups [26, 31], despite which we found no correlation in our series between sinus diameter and autograft regurgitation. Whether the autograft dilatation will stabilize or deteriorate further, eventually requiring autograft reoperation, as published by others [26, 32, 33], will only become apparent over time.
In this context, the reported advantage of the autograft implanted as a subcoronary root inclusion, hence stabilized by the patients' own aortic root, deserves renewed attention [15] and may be the preferable option in some patients with well-matched geometric dimensions of the autograft and the aortic root. Unfortunately, a substantial geometrical mismatch often exists between the pulmonary autograft and the obstructed LVOT, as in the Shone anatomic variation, or between the pulmonary autograft and the enlarged aortic annulus, for example, with a subaortic ventricular septal defect, in these pediatric patients. A full root replacement technique is mandatory in such cases to compensate for size and form differences [4]. We have paid particular attention to geometric mismatch between the autograft and the aortic annulus from the start of our experience with this operation and always allow for such differences in our surgical strategy [34].
The disturbing lack of durability of the pulmonary homografts used to reconstruct the right ventricular outflow tract is the major concern apparent in this series. Stenosis was the cause of reoperation in all 6 patients (6/60) who required reoperation and homograft replacement. The whole homograft conduit had shrunk in most patients, although occasionally a fibrotic ring was present at the proximal muscular portion of the homograft (Fig 3). In many the valve cusp tissue seemed preserved with minimal changes.
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Whether human leukocyte antigen (HLA) compatibility might influence homograft function and durability and, therefore, HLA-matching can improve homograft durability is still unclear, however [37]. Schmidtke and co-workers [38] made an interesting observation in this context. With the use of multivariate analysis, they found higher transvalvular homograft gradients during follow-up, depending on the number of packed red cells delivered perioperatively. Shaddy and colleagues [36] prophylactically treated their pediatric patients for 3 months with azathioprine as an immune suppressant after the implantation of cryopreserved homografts. The prospective trial published failed to demonstrate any influence on homograft stenosis or a reduction in the immune response to HLA alloantigens compared with controls [36]. This may offer promise as longer treatment becomes possible with less toxic and more specifically targeted drugs newly available in the field of transplantation.
The implantation of a decellularized cryopreserved homograft or stentless valve [39], eventually with use of tissue-engineering techniques to seed a homograft or stentless prosthesis with autologous cells, might be an alternative. Despite encouraging early results [40], long-term studies are awaited. There are justified concerns that any chemical or enzymatic decellularization process itself might damage homografts or stentless valve prostheses being treated in that way and lead to degeneration and failure of such valves. Dehiscence, rupture, and bleeding have been described in 3 patients in whom porcine heart valves prepared in this fashion were used [41]. The durable adherence of seeded cells, in conditions of pulsatile blood flow is problematic.
The sole use of porcine stentless prostheses for reconstruction of the RVOT is a further possible therapeutic approach occasionally reported, but long-term or even mid-term results are unavailable [42]. Our current policy is to strive for an adult-sized homograft in all patients, generally larger than 23 mm, and matched for blood group. If a child has received a homograft in the aortic position or elsewhere previously, antibodies are sought. If present, HLA typing is performed and a matched homograft from a beating heart donor with known tissue type and an acceptable tissue match is sought. At re-replacement, we avoid tension on the homograft and incorporate a scalloped Hemashield strip as an interposition between the host right ventricle and the homograft as a barrier to pannus or scar tissue.
As we have previously reported, almost all adult patients who underwent the Ross procedure at our institution have stable autograft and homograft function, approaching a cure for aortic valve disease [43]. In the current report on young recipients of the Ross operation, we documented inferior results to those achieved in adults, albeit results superior to those generally reported for alternative prostheses in children.
In conclusion, the Ross operation can be performed with good results, autograft function, and low mortality in young patients and achieves a better quality of life unencumbered by systemic anticoagulation, but the results are inferior to those achieved in adult patients. Pulmonary homograft durability is still unpredictable and also poorer than in adult patients. Physiologic autograft hemodynamics, potential growth, freedom from anticoagulation, and at least the shortcomings of conventional prostheses all justify continued use of the Ross operation in the young at specialized centers. The complexity of the operation and the absence of an ideal replacement for the autograft, with the mid-term reoperation rate of 10% for young Ross recipients, particularly due to pulmonary homograft dysfunction, remain limiting factors.
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