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J Thorac Cardiovasc Surg 2008;136:623-630
© 2008 The American Association for Thoracic Surgery
Surgery for Acquired Cardiovascular Disease |
Department of Surgery, Section of Thoracic and Cardiovascular Surgery, University of Oklahoma Health Sciences Center, Oklahoma City, Okla
Received for publication April 18, 2005; revisions received October 29, 2007; accepted for publication February 25, 2008. * Address for reprints: Ronald C. Elkins, MD, Section of Thoracic Surgery, University of Oklahoma Health Sciences Center, PO Box 26901, Oklahoma City, OK 73190. (Email: ronald-elkins{at}ouhsc.edu).
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionConclusionFigure E1Figure E2Figure E3Figure E4Figure E5References |
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Methods: We performed a prospective review of consecutive patients from August 1986 through June 2002 and follow-up through August 2004. Patient age was 2 days to 62 years (median, 24 years), and 197 patients were less than 18 years of age. The Ross operation was performed as a scalloped subcoronary implant in 26 patients, an inclusion cylinder in 54 patients, root replacement in 392 patients, and root–Konno procedure in 15 patients. Clinical follow-up in 96% and echocardiographic evaluation in 77% were performed within 2 years of closure.
Results: Actuarial survival was 82% ± 6% at 16 years, and hospital mortality was 3.9%. Freedom from autograft failure (autograft reoperation and valve-related death) was 74% ± 5%. Male sex and primary diagnosis of aortic insufficiency (no prior aortic stenosis) were significantly associated with autograft failure by means of multivariate analysis. Freedom from autograft valve replacement was 80% ± 5%. Freedom from endocarditis was 95% ± 2%. One late thromboembolic episode occurred. Freedom from allograft reoperation or reintervention was 82% ± 4%. Freedom from all valve-related events was 63% ± 6%. In children survival was 84% ± 8%, and freedom from autograft valve failure was 83% ± 6%.
Conclusions: The Ross operation provides excellent survival in adults and children willing to accept a risk of reoperation. Male sex and a primary diagnosis of aortic insufficiency had a negative effect on late results.
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionFigure E1Figure E2Figure E3Figure E4Figure E5References |
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Dissatisfaction with available options for aortic valve replacement in children and young adults led us to initiate the use of the Ross operation in August 1986. Clinical evaluation and echocardiographic surveillance at completion of the operation, 3 months postoperatively, 6 months postoperatively, and annually thereafter was planned. Although the initial operations were done as scalloped subcoronary implants, we rapidly changed to the modified subcoronary implant or root replacements in selected patients. Subsequent success with the root replacement led to its use in almost all patients. The use of the Ross operation has expanded to patients with complex left ventricular outflow tract obstruction, patients with active endocarditis, and the newborn. Prior reviews of this prospective study identified mechanisms of early failure and led to alterations in the procedure for management of patients with significant aortic insufficiency (AI), aortic annular dilation, and ascending aortic disease.1,2
This article addresses questions about the durability and operative risk of the Ross operation and the preferred operative technique, in particular the risk of progressive dilation of the autograft root and failure of the allograft reconstruction of the right ventricular outflow tract. We report the long-term results at a single institution during the period when use of the Ross operation expanded worldwide and seek to identify operative techniques and patient characteristics associated with survival and autograft valve durability.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionFigure E1Figure E2Figure E3Figure E4Figure E5References |
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The numbers of Ross operations and of all other aortic valve replacements for each year of the study are shown in Figure E1. Patient characteristics and preoperative clinical information are summarized in Table 1 . The autograft valve was inserted as a modified scalloped subcoronary implant in 26 patients, an inclusion cylinder in 54 patients, a root replacement in 392 patients, and a root–Konno procedure in 15 patients. The right ventricular outflow tract was reconstructed with a pulmonary allograft in 484 patients and an aortic allograft in 3 patients for whom a pulmonary allograft was unavailable. Operative findings concerning aortic valve morphology, aortic annulus dilation, or disease of the ascending aorta and management of these abnormalities are listed in Table 2 .
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Annual echocardiographic surveillance after the first postoperative year was planned. However, with continued follow-up, many patients' physicians elected to obtain echocardiograms every 2 or 3 years when their clinical evaluation did not indicate the need for annual assessment. Echocardiograms obtained at the University of Oklahoma Health Sciences Center were reviewed by echocardiographers with a special interest in the patients undergoing the Ross operation. Echocardiograms obtained from outside physicians were reread at the University of Oklahoma Health Sciences Center if they reported significant alteration in autograft or allograft function. Autograft valve insufficiency (AGI) was graded by using the thickness of the regurgitant stream relative to the size of the left ventricular outflow tract3 (0, none or trivial; 1+, mild; 2+, moderate; 3+, moderate–severe; and 4+, severe). Patient migration, loss of health insurance, or both decreased late echocardiographic surveillance. Echocardiographic assessment was available within 2 years of study closure in 2004 in 77% of the patients.
All analyses were performed with SAS System software, version 9.1 (SAS Institute, Inc, Cary, NC). Actuarial survival estimates of freedom from postoperative events were calculated by using Kaplan–Meier method, with differences assessed with the Wilcoxon and log-rank tests. All P values are reported. Cox multiple proportional hazards regression analyses were applied to time to autograft valve failure (AGF) and allograft valve failure (ALF).
Two-dimensional echocardiographic measurements of the diameter of the autograft root or autograft sinus (in millimeters) were recorded over time for each patient. Each measurement was z-transformed by using a regression equation4,5 that predicts the mean and standard deviation (root mean square of regression) for the diameter of the aortic sinuses of Valsalva for a given body surface area (BSA). BSAs were calculated by using the technique of Haycock and colleagues.6 The z-transformed autograft sinus diameters were subjected to longitudinal analysis in a general linear mixed model that accounted for correlation among an individual's measurements over time. The analysis was restricted to 383 patients who underwent a root replacement, for whom we collected 2147 echocardiographic measurements of root size. The model predicted z-transformed diameters after adjusting for a variety of fixed (between-subject) effects that appear to influence either sinus diameter at the time of surgical intervention or the rate of increase in diameter over time. Effects considered were age, sex, valve morphology, preoperative active endocarditis, primary hemodynamic lesion of aortic stenosis (AS) or AI (no prior AS), ventricular septal defect (VSD; subaortic), coarctation, ascending aortic dilation or aneurysm, prior median sternotomy, prior aortic valve replacement, annular fixation, aortic balloon valvuloplasty, and severity of AGI at completion of the operation. A backward selection technique eliminated variables until those remaining were significant.
Population-average changes in AGI over time were modeled with generalized estimating equations (GEEs) in the 469 operative survivors (3654 echocardiograms). Postoperative observations were truncated at the date of autograft reoperation for 38 patients, 10 of whose reoperations were unrelated to AGI. Predictions were calculated with SAS PROC GENMOD by specifying a cumulative logit model that accounted for repeated observations within subjects. Changes over time in AGI were investigated for the following predictors of outcome: implant technique, age (as a continuous variable), sex, aortic valve morphology, preoperative active endocarditis, primary preoperative hemodynamic lesion of AS or AI (no prior evidence of AS), VSD (subaortic), coarctation, ascending aortic dilation or aneurysm, prior median sternotomy, previous aortic valve replacement, annular fixation, aortic balloon valvuloplasty, and severity of AI at the completion of operation. These variables were entered simultaneously into the longitudinal model and then eliminated one by one until all variables remaining had a P value of .1 or less.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionFigure E1Figure E2Figure E3Figure E4Figure E5References |
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Survival (all causes) among the 487 patients was compared with the survival of the general US population, matched by each patient's age, sex, and year of operation (Figure 1 ). After the initial decrease associated with early hospital deaths, the survival appears to parallel the survival of the matched population to 13 years. After 13 years, the number of patients available for comparison is less than 10% of the surgical cohort. The confidence limits of the cohort's survival curve widen, limiting the validity of the later comparisons.
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AGF occurred in 46 patients (38 autograft valve reoperations, 2 valve-related deaths, and 6 sudden unexplained deaths that were counted as valve related). Table 3 identifies the primary causes for AGF requiring reoperation and the incidence of reoperation by initial operative technique. Autograft valve replacement was required in 27 of the 38 autograft valve reoperations, and the actuarial freedom from autograft valve replacement was 90% ± 2% and 80% ± 5% at 10 and 16 years, respectively.
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Autograft Root Dilation
Figure E3 displays the z-transformed autograft sinus or root diameter for all of the patients (383 operative survivors) who had a root replacement over time. Figure E4 displays mean observed and predicted values (derived from a general linear mixed model) for z-transformed autograft sinus or root diameters in this patient group. Although we planned to perform echocardiographs at specific postoperative intervals, the procedures' actual timing varied considerably. Observations were grouped to use each patient's multiple echocardiographic studies to calculate mean diameters at defined intervals.
The observed baseline (time = 0) mean z value of 1.97 ± 1.88 increases to a z value of 3.15 ± 2.18 at 1 year after the operation. Change thereafter is gradual. A general linear mixed model yielded estimates of aortic diameter that accounted for correlations among patients' repeated measurement over time. The predicted baseline z diameter of 1.96 is adjusted downward by 0.04 z units for each year of a patient's age at the time of the operation. Patients with a primary lesion of AI have baseline diameters that are 0.57 z units larger (P = .0026). Male subjects' baseline diameters are 0.40 z units larger than those of female subjects (P = .0389). The cohort included 30 patients with a subaortic VSD, whose diameters were marginally larger (1.35 z units, P = .058). No factors were associated with smaller baseline diameters.
The model separately estimated the rate of change in aortic diameter over the first 12 months and after 12 months. Diameter increased by 0.13 z units per month during the first 12 months. The predicted rate of change after 12 months is 0.019 z units per month (standard error, 0.0086; 95% confidence limit, 0.003–0.036).
Four factors were associated with a more rapid increase in diameter over the first 12 months: grade 2 (but not grade 1) baseline AI (an additional increase of 0.18 z units per month, P = .0249), bicuspid aortic valve (an additional 0.09 z units per month, P = .0010), a history of coarctation (an additional 0.09 z units per month, P = .0131), and repair of an aortic aneurysm as part of a Ross operation (an additional 0.06 z units pre month, P = .0047). After 12 months, these 4 factors were not associated with differences in the overall predicted rate of change of 0.019 z units per month.
Patients who had cuff fixation of their aortic annulus had a rate of change in aortic diameter over the first 12 months that was 0.058 z units per month slower than the others (P = .0086). After 12 months, their rate of change was 0.019 z units per month faster than (or about double the rate of those) without cuff fixation (P = .0005). We also investigated but found no interaction between sex and primary lesion of AI (P = .9) or between the bicuspid aortic valve and aneurysm (P = .4) with respect to rate of change in aortic diameter.
Valve Function
Changes over time in the severity of AGI, as observed and predicted by GEEs, are shown in Figure 3
. Because few patients had moderate–severe (3+) or severe (4+) AGI, these groups were combined for analysis. The predicted probability of no or trivial (grade 0) AGI decreased from 63% in the early postoperative period to 52% at 5 years, 36% at 10 years, and 24% at 16 years. The predicted probability of mild (grade 1) and moderate (grade 2+) AGI increased, with 50% having mild and 17% having moderate insufficiency at 16 years. A separate GEE analysis that focused only on the development of moderate–severe (3+) and severe (4+) AGI is shown in Figure 4
. Predicted 3+ or 4+ AGI slowly increased to 3.3% (70% confidence interval [CI], 2.7%–4%) at 5 years, 7.9% (70% CI, 5.8%–9.5%) at 10 years, and 21.5% (80% CI, 15.3%–29.4%) at 16 years.
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Thromboembolism
Thromboembolism was identified in only 1 patient who had a nonfatal coronary embolism during treatment for endocarditis. Six patients died suddenly and were presumed to represent valve-related deaths. One or more of these deaths might have been an unrecognized episode of thromboembolism. Anticoagulation was used only in patients who had an associated mitral valve procedure that required anticoagulation.
Allograft Valve Failure
ALF was defined as allograft valve reoperation or intervention. Actuarial freedom from ALF was 90% ± 2% at 10 years and 82% ± 4% at 16 years. Multivariable proportional hazard regression identified younger age at operation (P = .02; hazard ratio [HR], 0.97; 95% CI, 0.94–0.1), previous aortic valve replacement (P < .0001; HR, 6.23; 95% CI, 2.72–14.28), history of bacterial endocarditis (P = .002; HR, 4.58; 95% CI, 1.75–11.98), and male sex (P = .01; HR, 4.01; 95% CI, 1.39–11.56) as independent risk factors for increased ALF. Allograft valve replacement or intervention was required in 33 patients. Accelerated ALF within 1 year of allograft insertion occurred in 3 patients.
A number of patients with significant obstruction of the allograft conduit or allograft valve insufficiency are being followed. Allograft degeneration was defined as allograft reoperation or intervention, a peak allograft gradient of 50 mm Hg or more, or severe allograft valve insufficiency. Actuarial freedom from allograft degeneration was 81% ± 3% and 71% ± 5% at 10 and 16 years, respectively. Balloon valvuloplasty, stent placement, or both was performed in 7 patients, and in 5 of these, allograft replacement has not been required for up to 8 years after the intervention. Repeat intervention was required on 2 occasions in 2 patients.
Valve-related Morbidity
Valve-related morbidity is defined as AGF, ALF, endocarditis, and valve-related death. Actuarial freedom from valve-related morbidity was 80% ± 3% and 63% ± 6% at 10 and 16 years, respectively.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionFigure E1Figure E2Figure E3Figure E4Figure E5References |
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Operative Technique
The root replacement is the most versatile technique, allowing the surgeon to replace the aortic valve in patients of any age and to manage complicated left ventricular outflow tract obstructions. If the patient's pulmonary valve is normal, this technique is most likely to provide the patient with a competent autograft valve with minimal AGI at completion of the operation. The operation has an increased risk of intraoperative bleeding and a risk of malalignment of the coronary arteries at the time of implantation to the autograft root.
Our experience raises several technical and patient selection concerns. Autograft insufficiency was the most common cause of autograft reoperation. The most common cause of autograft insufficiency was late dilation of the autograft annulus, particularly in patients with AI as their primary lesion. We presently use aortic annulus fixation with synthetic material or glutaraldehyde-fixed pericardium in all older adolescents and adults whose BSA-standardized aortic annulus approaches a normal diameter. We reduce the aortic annulus if it is dilated. The only independent predictors of development of moderate–severe or severe AGI were increasing age at the time of the operation and AGI at completion of the operation and increasing follow-up time. Previous aortic valve replacement was protective.
Careful inspection of the pulmonary valve is essential before proceeding with a Ross operation. Use of a pulmonary valve with minor abnormalities will likely accelerate failure. Ross operations that were performed in 5 patients whose pulmonary valves had minor abnormalities all required replacement of the autograft valve at 2.9 to 8.5 years, with a median of 4 years. Still, use of the valve is acceptable in some very young children or adolescents in whom other alternatives are less acceptable.
Our experience supports the use of the Ross operation in the management of patients with aortic valve endocarditis. Forty patients had endocarditis that led to aortic valve replacement, and in 24 patients it was active. In patients with active endocarditis, appropriate antibiotic therapy was completed after surgical intervention, and late endocarditis was identified in 5 patients, all related to recurrent intravenous drug use. The Ross operation was remarkably free of hospital-acquired endocarditis, which occurred in only 1 patient because of an infected central venous catheter.
Recent concern centers on autograft failure caused by autograft root dilation, especially in patients with a bicuspid aortic valve.7 In our series aortic valve morphology was not a risk factor for AGF by means of univariate or multivariate analysis.
Using echocardiographic standards for aortic sinus and root diameters, several authors have identified significant increases in autograft sinus and root diameters,8-10 whereas others have shown limited dilation after the first postoperative year.11,12 The use of echocardiographic standards for the aortic root or sinuses might not be appropriate. Many adults and children have autograft sinus or root diameters that exceed the accepted aortic diameters early, when the autograft root distends at systemic pressure. Our general linear mixed-model analyses of z-transformed aortic sinus or root diameters demonstrated that bicuspid aortic valve, repair of an ascending aortic aneurysm, grade 2 early postoperative AI, and history of a subaortic VSD were associated with more rapid increases in diameter during the first 12 months of follow-up. However, after 12 months, patients displaying these characteristics exhibit very gradual changes in diameter that do not differ from those of the overall group.
The optimal timing for autograft reoperation for dilation is unclear. Recently, Ergin and colleagues13 and Gleason and associates14 have suggested that elective operation on the dilated ascending aorta should be based on a ratio of observed to predicted diameter rather than the absolute size. They suggest a ratio of 1.5 as an indication for replacement of a degenerative aorta with or without AI or at the time of other cardiac surgery compared with a ratio of 1.3 for an elective operation in a patient with Marfan syndrome. Autograft root dissection is rare, with only 5 reported cases,1,5,15-19 and we have recently performed a reoperation on a patient with severe autograft insufficiency and a 5.3-cm autograft root and identified an unexpected chronic dissection. Autograft rupture has not been reported.
Accepting the suggestions of Ergin and colleagues13 and Gleason and associates14 and using the equations that Roman and coworkers20 developed to predict diameters for the aortic root and sinus of Valsalva from BSA, we identified 86 patients in our series with at least 1 ratio (echocardiographically measured diameter/predicted diameter) greater than 1.5. Forty-seven patients had 2 or more ratios greater than 1.5. The trajectories of these individual patients are shown in Figure E5. Although most demonstrate consistent ratios over time, a few have progressive increases in their ratios and might be candidates for elective replacement of their autograft root by a valve-sparing operation or a root replacement. These suggestions are in contrast to those of Luciano and Mazzuco.21
Our data suggest that male subjects with primary AI have an increased risk for autograft failure and might have an increased risk of reoperation, but they are not at a greater risk for autograft root dilation. The excellent survival and absence of thromboembolism or hemorrhage complications and a very low risk of endocarditis might warrant recommendation of a Ross operation, but the patient must be made aware of the likely increased risk of reoperation.
Increasing concern about the incidence of dilation of the autograft root has caused many surgeons to reconsider the subcoronary implant or the inclusion cylinder technique. The use of the subcoronary and inclusion techniques requires careful matching of the size of the autograft root to the aortic annulus size, the sinus diameter, and the sinotubular diameter of the aortic root. The autograft root is very distensible, and its size is probably best calculated from measurement of the diameter of the sinotubular ridge of the pulmonary root.22 The subcoronary and inclusion cylinder techniques cannot be used in patients who require replacement or reconstruction of the proximal aortic root or in patients who require a Ross–Konno procedure for management of left ventricular outflow tract obstruction. Also, infants and young children can rarely have a Ross operation as a subcoronary implant or as an inclusion cylinder because of the small size of the aortic annulus.
Reconstruction of the Right Ventricular Outflow Tract
Pulmonary allografts were our choice for reconstruction of the right ventricular outflow tract. We based allograft size on patient age and used an allograft that was larger than the predicted pulmonary valve size based on BSA. When possible, allografts from donors with the blood type of the recipient were used. Previous multivariate analysis has shown young donor age, later year of operation, and non-Ross operation as risk factors for allograft failure.23 Raanani and associates24 identified younger donor age, shorter duration of cryopreservation, and smaller allograft size as independent predictors of late allograft stenosis in 109 patients undergoing the Ross operation. Both of these studies suggest that an immune-mediated response can be associated with allograft failure. Accelerated allograft failure caused by an immune-mediated response has been demonstrated in aortic allografts25 and pulmonary allografts in children.26
Alternative approaches to the management of right ventricular outflow tract reconstruction have been introduced. Novick and colleagues27 have had early good results with the use of the freestyle porcine aortic root in 11 patients undergoing the Ross operation. Purohit and coworkers28 reported good early results in 20 patients undergoing the Ross operation using the Contegra bovine jugular vein conduit for right ventricular reconstruction. Results with both approaches are encouraging, but significant follow-up must be obtained before their adoption as an improvement over the allograft.
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Conclusion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionFigure E1Figure E2Figure E3Figure E4Figure E5References |
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although this comparison is limited by our inability to have complete echocardiographic follow-up. The only clinical parameters that clearly affect autograft degeneration are male sex and a primary diagnosis of AI. Aortic annulus fixation and reduction, when indicated, appear to delay the occurrence of autograft failure and might reduce the incidence. The role of sinotubular junction fixation, advocated by some, was not addressed in this study. Autograft root dilation remains a concern and might limit the xapplicability of the root replacement. Presently accepted standards for replacement of a dilated degenerative ascending aorta might be too conservative for the autograft root. Allografts remain the gold standard for right ventricular reconstruction. However, the development of a viable and durable means of reconstruction of the right ventricular outflow tract is needed. Lifetime echocardiographic surveillance should be maintained on all patients.
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Figure E1 |
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Figure E2 |
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Figure E3 |
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Figure E4 |
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Figure E5 |
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Footnotes |
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References |
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G. B. Luciani, F. Viscardi, M. Pilati, A. M. Prioli, G. Faggian, and A. Mazzucco The Ross-Yacoub procedure for aneurysmal autograft roots: A strategy to preserve autologous pulmonary valves J. Thorac. Cardiovasc. Surg., March 1, 2010; 139(3): 536 - 542. [Abstract] [Full Text] [PDF]
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T. E. David, A. Woo, S. Armstrong, and M. Maganti When is the Ross operation a good option to treat aortic valve disease? J. Thorac. Cardiovasc. Surg., January 1, 2010; 139(1): 68 - 75. [Abstract] [Full Text] [PDF]
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E. I. Charitos, T. Hanke, U. Stierle, D. R. Robinson, A. J.J.C. Bogers, W. Hemmer, M. Bechtel, M. Misfeld, A. Gorski, J. O. Boehm, et al. Autograft Reinforcement to Preserve Autograft Function After the Ross Procedure: A Report From the German-Dutch Ross Registry Circulation, September 15, 2009; 120(11_suppl_1): S146 - S154. [Abstract] [Full Text] [PDF]
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J. Horer, T. Hanke, U. Stierle, J. J.M. Takkenberg, A. J.J.C. Bogers, W. Hemmer, J. G. Rein, R. Hetzer, M. Hubler, D. R. Robinson, et al. Neoaortic Root Diameters and Aortic Regurgitation in Children After the Ross Operation Ann. Thorac. Surg., August 1, 2009; 88(2): 594 - 600. [Abstract] [Full Text] [PDF]
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J. W. Brown, M. Ruzmetov, A. Shahriari, M. D. Rodefeld, Y. Mahomed, and M. W. Turrentine Midterm Results of Ross Aortic Valve Replacement: A Single-Institution Experience Ann. Thorac. Surg., August 1, 2009; 88(2): 601 - 608. [Abstract] [Full Text] [PDF]
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T. E. David Ross Procedure at the Crossroads Circulation, January 20, 2009; 119(2): 207 - 209. [Full Text] [PDF]
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