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Ann Thorac Surg 2004;78:773-781
© 2004 The Society of Thoracic Surgeons
a Division of Cardiovascular and Thoracic Surgery, Missouri Baptist Medical Center, MO, USA
b Division of General Medical Sciences and Biostatistics,St. Louis, MO, USA
c Cardiovascular Imaging and Clinical Research Core Laboratory, Cardiovascular Division, Washington University School of Medicine, St. Louis, Missouri, USA
Accepted for publication February 10, 2004.
* Address reprint requests to Dr Kouchoukos, Cardiac, Thoracic and Vascular Surgery, Inc, 3009 N Ballas Rd, St. Louis, MO 63131, USA
ntkouch{at}aol.com
Presented at the Fiftieth Annual Meeting of the Southern Thoracic Surgical Association, Bonita Springs, FL, Nov 13–15, 2003.
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Abstract |
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 Top Abstract IntroductionMaterial and methodsResultsEchocardiographic studiesCommentAddendumDiscussionReferences |
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METHODS: A Ross procedure was performed on 119 older children and young adults (mean age: 31 years old), using the root replacement technique, between June 1989 and January 2002. Serial echocardiography studies were obtained in 108 patients and analyzed blinded to clinical data. The following variables were measured: diameter of annulus, sinuses of Valsalva, and supravalvular ridge; presence and severity of aortic regurgitation; and valve thickening.
RESULTS: The 30 day and late mortality rates were 1.7% and 1.7% (2 patients each). Forty-one patients were followed for more than 5 years, 19 for more than 7 years, and 9 for more than 10 years. There was one thrombotic and no endocarditis events. The 10-year actuarial survival was 96%. Reoperation on the pulmonary autograft or the pulmonary allograft was required in 12 patients. The principal indication for operation on the pulmonary autograft in 11 patients was neo-aortic valve regurgitation (7), aneurysm formation (3), and false aneurysm (1). At 10 years, actuarial freedom from reoperation on the pulmonary autograft was 75%. At last follow-up, 8 of 97 patients without reoperation on the autograft had moderate and none had severe regurgitation of the neo-aortic valve. Independent predictors of progression of neo-aortic valve regurgitation were time from operation, dilatation of the supravalvular ridge, and neo-aortic valve thickening (all p < 0.0002). Freedom from reoperation in the pulmonary allograft at 10 years was 86%.
CONCLUSIONS: Long-term follow-up of patients with the Ross procedure using the root replacement technique indicates excellent survival and low thromboembolic and endocarditis risk. The main limitation is the need for reoperation. The prevalence of severe neo-aortic valve regurgitation is low, however there is a progressive increase in regurgitation and in aortic root diameters. Periodic follow-up with echocardiography is recommended because of the continuing risk of progressive regurgitation of the neo-aortic valve and aneurysm formation.
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Introduction |
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TopAbstractIntroductionMaterial and methodsResultsEchocardiographic studiesCommentAddendumDiscussionReferences |
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Material and methods |
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TopAbstractIntroductionMaterial and methodsResultsEchocardiographic studiesCommentAddendumDiscussionReferences |
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Preoperative evaluation
In addition to echocardiographic and other noninvasive studies, all adult patients underwent left-heart catheterization and coronary arteriography to assess the severity of the aortic valve disease and left ventricular dysfunction, to detect the presence of coronary arterial occlusive disease, and to determine the size and number of proximal septal perforating branches of the anterior descending coronary artery. Large conal branches of the right coronary artery, which could be injured during removal of the pulmonary root, were also identified.
Operative procedure
Our technique for aortic root replacement with a pulmonary autograft and for reconstruction of the right ventricular outflow tract has been previously reported [3]. Intraoperative transesophageal two-dimensional and color flow Doppler transesophageal echocardiography (TEE) was performed in all but the youngest patients to measure the diameter of the aortic and the pulmonary annulus and to assess the competence of the pulmonary valve. The diameter of the annulus of the pulmonary valve was also measured after excision of the valve using a conical sizer. Patients with marked dilatation of the aortic sinuses or with an annulus that measured more than 30 mm were not considered candidates for the procedure. In the majority of patients, the diameter of the aortic annulus did not exceed the diameter of the pulmonary annulus by more than 2 to 3 mm. In 7 patients, plicating sutures were placed in the aortic commissures to reduce the diameter of the aortic annulus so that it approximated the diameter of the autograft. A strip of polytetrafluoroethylene (PTFE) felt or autologous pericardium was used to reinforce the suture line between the pulmonary autograft and the aortic annulus in all of the older children and adults. A strip of PTFE felt was also used to reinforce the anastomosis between the pulmonary autograft and the ascending aorta in 65 of 119 patients. This anastomosis was performed as close as possible to the sinotubular junction of the autograft. The right ventricular outflow tract was replaced with a pulmonary allograft in every patient. A graft with a diameter larger than the diameter of the native pulmonary valve was used to reduce the risk of development of pulmonary stenosis. The allografts were not matched to the blood type of the patient.
The mean duration of cardiopulmonary bypass was 192 minutes (range, 87 to 454 minutes). During the period of myocardial ischemia, which averaged 149 minutes (range, 54 to 222 minutes), the myocardium was protected by intermittent infusion of a cold blood cardioplegic solution directly into the coronary ostia or retrogradely into the coronary sinus. External cooling of the heart was accomplished with a cooling jacket or topical slush. After discontinuation of cardiopulmonary bypass, the competence of the pulmonary autograft valve and the pulmonary allograft valve in the right ventricular outflow tract was assessed by TEE.
Associated procedures
In addition to the 15 patients who had replacement of the ascending aorta, 4 patients had replacement of the proximal aortic arch, 2 had repair of the mitral valve, and 1 each had coronary artery bypass grafting, closure of a patent ductus arteriosus, repair of a coronary sinus-to- right atrial fistula, left ventricular septal myectomy, and repair of a foramen of Morgagni hernia.
Postoperative evaluation and management
Transthoracic M-mode, two-dimensional, color-flow, and Doppler echocardiograms were obtained before discharge from the hospital and at 6 to 12 month intervals thereafter. The severity of neo-aortic valve regurgitation (AR) was measured using a modification of the method of Perry and colleagues [8], in which the ratio of the width of the jet of regurgitation to the diameter of the left ventricular outflow tract just below the level of the valve annulus is determined. The regurgitation was graded as follows: no AR, no diastolic color flow; trivial AR, ratio more than 0 but less than 0.2; mild AR, ratio of 0.2 to 0.29; mild to moderate AR, ratio of 0.3 to 0.39; moderate AR, ratio of 0.4 to 0.49; moderate to severe AR, ratio of 0.5 to 0.59; and severe AR, ratio more than 0.6. A numerical grade was assigned to these ranges (Table 1). Using the method of Roman and coworkers [9], three dimensions of the pulmonary root autograft at end-diastole were measured: the diameter of the annulus, the maximal diameter of the sinuses of Valsalva, and the diameter at the supravalvular ridge. Thickening of the valve leaflets was qualitatively determined using a scale of 1 to 4 (1 = normal, 4 = severe valve thickening). The peak velocity of flow across the pulmonary autograft and pulmonary allograft valves was also measured, and gradients were estimated using the modified Bernoulli equation. The echocardiograms were interpreted by a single cardiologist who was blinded to the clinical status of the patients.
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No anticoagulants were administered to any of the patients after operation. Use of platelet antiaggregating agents in the follow-up period was left to the discretion of the attending cardiologist. The mean duration of follow-up for the entire cohort was 4.4 years (range, 10 months to 13 years). The date of last inquiry was October 2002.
Statistical analysis
Paired t-testing and pertinent mixed models analysis were used to determine changes in diameter of the neo-aortic root over time using SAS programs (Cary, NC). Stepwise linear regression analysis was performed to identify variables predictive of neo-aortic valve regurgitation. A p value less than 0.05 was considered statistically significant. Survival and event-free analyses were performed using the Kaplan-Meier method.
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Results |
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Ventricular dysrhythmias requiring drug therapy occurred in 21 patients (18%). One patient required implantation of a permanent pacemaker. Seven patients had low output syndrome. Two of these patients required insertion of ventricular assist devices and did not survive. One of the remaining 5 patients had insertion of an intraaortic balloon pump, and all survived. One patient developed a temporary partial homonymous hemianopsia. The mean and median postoperative lengths of stay in the hospital were 6 and 7 days respectively (range, 3 to 47 days).
One patient with Libman-Sacks endocarditis and the presence of antiphospholipid antibody, sustained a cerebral embolic event 9 months postoperatively and warfarin therapy was initiated at that time. No other patient sustained a postoperative embolic event. The actuarial freedom from thromboembolism at 10 years was 99%. No patient developed endocarditis of the autograft or the pulmonary allograft.
Reoperation
Reoperation on the pulmonary autograft or the pulmonary allograft was required in 12 patients (Table 2). The time interval between the initial procedure and the reoperation ranged from 2 to 140 months. Eight patients underwent reoperation on the pulmonary autograft, 3 patients on the autograft and the pulmonary allograft, and 1 patient on the pulmonary allograft. The principal indication for replacement of the 11 pulmonary autografts was regurgitation of the neo-aortic valve in 7, aneurysm of the pulmonary arterial component of the autograft in 3 (with or without associated regurgitation), and false aneurysm in 1 patient. In 2 of 9 patients with neo-aortic valve regurgitation, perforation of a leaflet, likely related to injury at the time of implantation, was a major cause of the regurgitation. In the remaining 7 patients, the regurgitation was associated with dilatation of the neo-aortic root and separation of the valve leaflets. Only 3 of 11 procedures to replace or repair the pulmonary autograft were performed in the first 5 postoperative years. The remaining 8 procedures were performed from 62 to 140 months following the initial operation.
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At 5, 7, and 10 years postoperatively, freedom from reoperation on the pulmonary autograft was 95%, 80%, and 75% respectively (Fig 2), and freedom from reoperation on the pulmonary allograft was 99%, 92%, and 86% respectively (Fig 3). The procedures performed at the time of reoperation are shown in Table 2. All but one of the 12 patients survived reoperation and these 11 patients were all alive at the date of last follow-up. Event-free survival (freedom from death, reoperation, thromboembolism, and endocarditis) was 93% at 5 years, 78% at 7 years, and 73% at 10 years postoperatively (Fig 4).
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Echocardiographic studies |
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Comment |
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TopAbstractIntroductionMaterial and methodsResultsEchocardiographic studiesCommentAddendumDiscussionReferences |
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Multiple causes for reoperation have been identified with the root replacement technique. These include technical problems such as injury to the neo-aortic valve at the time of implantation, geometric mismatch, false aneurysm, infection, immunologically mediated injury, and structural changes in the autograft that predispose to dilatation of the autograft with development of aortic regurgitation and aneurysm formation. Progressive dilatation of the native aorta adjacent to the autograft may also result in regurgitation of the neo-aortic valve because of dilatation at the site of anastomosis of the aorta to the autograft. This latter change can occur with the subcoronary, root inclusion, or root replacement techniques. In our study, which involved use of only the root replacement technique, dilatation of the autograft with progressive neo-aortic valve regurgitation was the most common indication for reoperation.
When the root replacement technique is used, serial echocardiographic studies have demonstrated progressive enlargement of the autograft over time [5–7, 10, 16, 17]. The dilatation has been most pronounced at the sinus and sinotubular levels. In our series, no substantial dilatation occurred at the annular level (Table 4). This could be due to use of a band of PTFE or autologous pericardium that reinforced the suture line. However, dilatation at the level of the sinuses and the sinotubular junction was significant and progressive, continuing for up to 10 years postoperatively. Although this dilatation was not consistently associated with the development or progression of neo-aortic valve regurgitation, the diameter of the sinotubular ridge was an independent predictor for the development of AR.
Structural changes in the wall of the autograft and in the valve leaflets are likely an important contributing factor to development of dilatation and valve regurgitation when the root replacement technique is used [18–20]. In a histologic study of two of the autografts in our series that were replaced at 52 and 80 months postoperatively, considerable transmural injury of the arterial wall was evident, with loss of medial smooth muscle cells and elastin and variable degrees of scarring, without inflammation or calcification [20]. Similar findings in two patients were reported by Takkenberg and colleagues [19].
Whether progressive neo-aortic valve regurgitation and dilatation of the pulmonary autograft can be minimized or prevented by alternative techniques for implantation is not known with certainty. A follow-up study of the pioneer series of Donald Ross reported by Chambers and associates [1] demonstrated that neo-aortic valve regurgitation was the most common indication for reoperation. Among 131 hospital survivors, 30 patients required late reoperations, and 28 of these procedures were performed for severe regurgitation. Freedom from reoperation was similar for the 107 patients in whom the subcoronary technique was used and for the 20 patients in whom the root replacement technique was used. In a more recent study, Sievers and coworkers [15] reported their experience with the subcoronary technique in 228 patients and with the root inclusion technique in 17 patients who were followed for a mean of 29 months. The reoperation rate on the autograft in the first 2 years was comparable to that reported by Chambers and associates [1].
Experience with the root inclusion technique is less extensive. Although use of this technique may prevent dilatation of the annulus and the neo-aortic sinuses, it will not prevent progressive dilatation of the supravalvular aorta unless the ascending aorta is replaced or reinforced. Elkins and colleagues [2] reported a significantly lower rate of freedom from reoperation and substantial neo-aortic valve regurgitation among the 86 patients with an intraaortic procedure (60 root inclusion, 26 subcoronary) than among the 242 patients in whom the root replacement technique was used. Modification of the root inclusion technique by fixation of the aortic annulus and the sinotubular junction reported by Skillington and coworkers [21] and David and associates [5] may improve the outcomes. However, long-term follow-up information from these series is not available. Malposition and distortion of the mobilized coronary arteries and other technical problems may be limitations to the widespread use of this technique [22].
Continued follow-up has confirmed earlier observations that moderate pressure gradients develop across the pulmonary allografts in the right ventricular outflow tract [3, 15, 23]. Patients with substantial gradients require reoperation [1, 3, 15, 23]. In our series, one patient required reoperation for isolated stenosis of the pulmonary allograft, and two additional patients had the allograft replaced for stenosis in combination with replacement of the pulmonary autograft valve (Table 2). Freedom from reoperation on the pulmonary allograft was 86% at 10 years.
In conclusion, extended follow-up of young patients having the Ross procedure using the root replacement technique has demonstrated excellent survival with minimal risk for thromboembolism and endocarditis. Progressive dilatation of the autograft and regurgitation of the neo-aortic valve that require reoperation remain the principal limitations of the procedure. Reoperation for these complications was performed more frequently in the second 5-year interval of follow-up than in the first 5 years, and was required as late as 12 years postoperatively. Because of these continuing risks, periodic evaluation of all patients with echocardiography is recommended.
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Addendum |
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Discussion |
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TopAbstractIntroductionMaterial and methodsResultsEchocardiographic studiesCommentAddendumDiscussionReferences |
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I have recently reviewed our patients, age 0 to 17 years, as I am presenting a paper on these patients next week. In this group of patients, we have an actuarial freedom from re-operation on the autograft valve of 94% at 12 years, if the pulmonary valve was normal at the time we did the operation. We have had excellent hemodynamic results in these patients. We are concerned as you are about the possibility of progressive dilatation.
We have done a multivariate analysis of the results in these patients, and the only indicator that predicts re-operation on the autograft valve is a primary lesion of aortic insufficiency (AI), not a patient who had AI because he had a balloon valvuloplasty or a previous aortic procedure for aortic stenosis but a primary lesion of AI. In that group of patients, the Ross operation may not be the appropriate procedure if you have another alternative, because at 12 years their freedom from re-operation is 64%, a significant failure rate in these patients.
We have not completed the analysis similar to yours. I am going back and relook at the change in pulmonary autograft root size over time in our patients. I think it is probably not different than yours. This is an outstanding paper and we appreciate your presentation. Thank you.
DR KOUCHOUKOS: I think it is important if we are going to continue to perform the Ross procedure, that we attempt to identify the risk factors for dilatation and for progressive aortic regurgitation. If the patients can be more appropriately selected, the long-term results will be better.
DR ROSS M. UNGERLEIDER (Portland, OR): Doctor Kouchoukos, that is a wonderful follow-up and very helpful. We have had a similar experience of about 160 Ross procedures on children and adults between both Duke and now in Oregon. We have had very limited amounts of autograft dilatation, but I was interested in the fact that 66% of your patients had bicuspid aortic valves, and we have been a little bit worried about the patients who present with bicuspid aortic valves and dilated aortas to begin with, and in those patients we have elected to replace the aortic valve with an autograft and the ascending aorta with a Dacron graft.
The one patient that had dilatation and failure of his autograft in our series had a bicuspid aortic valve with an aneurysm of the aorta at presentation and we didn't do that, and since then with selective graft implantation for those patients we have haven't had a failure, but I don't know what that means; our follow-up is only out to about 15 years.
I am curious if you had any thoughts about those types of patients, that is, the patients who present with dilated aortas and bicuspid aortic valves? Does that constitute a risk for eventual autograft dilatation? Do you manage these patients with a Dacron interposition graft in the aorta and if so, has that altered the long- term outcome?
DR KOUCHOUKOS: Because of the limitations of time, I did not present information on that issue. Fifteen of the patients in our series had aneurysmal dilatation of their ascending aorta at the time of the initial procedure and had the ascending aorta replaced with a polyester graft. We have looked at those patients, and 2 of the 15 have required reoperation. Although one would hope that there would be less of a problem with dilatation of the autograft in this setting, I am not certain that replacing the ascending aorta will totally avoid this problem.
DR THORALF SUNDT (Rochester, MN): Doctor Kouchoukos, what advice do you have for us at the reoperation? Last week I had occasion to do the sixth aortic valve operation on a 35-year-old woman. It can be a tough lie if they have had a previous Ross and revisions thereof. You have said what you did with two of your patients at redo. What advice do you have for us if we are confronted with a patient with a previous Ross in terms of the procedure that ought to be done and what advice would you offer about the pulmonary homograft at that time?
DR KOUCHOUKOS: Well, the first piece of advice I would give would be not to do a Ross operation when it is the fifth or sixth procedure on the aortic valve. Clearly, reoperations are associated with increased risk. We have been fortunate that the 12 reoperations in our series resulted in only one death. This patient was operated upon two months after the Ross operation for a false aneurysm. We suspected infection but this was never proven. Of the remaining 11 reoperations, two were valve sparing procedures, one was an isolated replacement of the pulmonary allograft, and the remainder were aortic root or aortic valve replacements with or without replacement of the pulmonary allograft.
One has to approach these reoperations with the same precautions as those taken for the other reoperations on the aortic root or ascending aorta. The pulmonary allograft is also at risk for injury, and it is important to know the location of a dilated autograft or pulmonary allograft before dividing the sternum.
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L. M.A. Klieverik, J. J.M. Takkenberg, B. C.J. Elbers, F. B.S. Oei, L. A. van Herwerden, and A. J.J.C. Bogers Dissection of a dilated autograft root J. Thorac. Cardiovasc. Surg., March 1, 2007; 133(3): 817 - 818. [Full Text] [PDF]
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P. H. Schoof, J. J.M. Takkenberg, R.-J. van Suylen, P. E. Zondervan, M. G. Hazekamp, R. A.E. Dion, and A. J.J.C. Bogers Degeneration of the pulmonary autograft: An explant study J. Thorac. Cardiovasc. Surg., December 1, 2006; 132(6): 1426 - 1432. [Abstract] [Full Text] [PDF]
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 R. Wang, A. Farnsworth, and H. Albrecht Mid-term results of ross procedure: our limited experience. Asian Cardiovasc Thorac Ann, August 1, 2006; 14(4): 289 - 293. [Abstract] [Full Text] [PDF]
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H. H. Sievers, T. Hanke, U. Stierle, M. F. Bechtel, B. Graf, D. R. Robinson, and D. N. Ross A Critical Reappraisal of the Ross Operation: Renaissance of the Subcoronary Implantation Technique? Circulation, July 4, 2006; 114(1_suppl): I-504 - I-511. [Abstract] [Full Text] [PDF]
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M. H. Yacoub The Ross Operation - An Evolutionary Tale Asian Cardiovasc Thorac Ann, February 1, 2006; 14(1): 1 - 2. [Full Text] [PDF]
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A. Sampath Kumar, S. Talwar, A. Saxena, and R. Singh Ross procedure in rheumatic aortic valve disease Eur. J. Cardiothorac. Surg., February 1, 2006; 29(2): 156 - 161. [Abstract] [Full Text] [PDF]
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D. G. Pennington The Impact of New Technology on Cardiothoracic Surgical Practice Ann. Thorac. Surg., January 1, 2006; 81(1): 10 - 18. [Full Text] [PDF]
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G. B. Luciani, A. Favaro, G. Casali, F. Santini, and A. Mazzucco Ross Operation in the Young: A Ten-Year Experience Ann. Thorac. Surg., December 1, 2005; 80(6): 2271 - 2277. [Abstract] [Full Text] [PDF]
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T. Karamlou, K. Jang, W. G. Williams, C. A. Caldarone, G. Van Arsdell, J. G. Coles, and B. W. McCrindle Outcomes and Associated Risk Factors for Aortic Valve Replacement in 160 Children: A Competing-Risks Analysis Circulation, November 29, 2005; 112(22): 3462 - 3469. [Abstract] [Full Text] [PDF]
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E. G. Butchart, C. Gohlke-Barwolf, M. J. Antunes, P. Tornos, R. De Caterina, B. Cormier, B. Prendergast, B. Iung, H. Bjornstad, C. Leport, et al. Recommendations for the management of patients after heart valve surgery Eur. Heart J., November 2, 2005; 26(22): 2463 - 2471. [Abstract] [Full Text] [PDF]
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J. J.M. Takkenberg, A. P. Kappetein, L. A. van Herwerden, M. Witsenburg, L. V. Osch-Gevers, and A. J.J.C. Bogers Pediatric Autograft Aortic Root Replacement: A Prospective Follow-Up Study Ann. Thorac. Surg., November 1, 2005; 80(5): 1628 - 1633. [Abstract] [Full Text] [PDF]
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 I. Vesely Heart Valve Tissue Engineering Circ. Res., October 14, 2005; 97(8): 743 - 755. [Abstract] [Full Text] [PDF]
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L. G. Svensson and E. R. Rodriguez Aortic Organ Disease Epidemic, and Why Do Balloons Pop? Circulation, August 23, 2005; 112(8): 1082 - 1084. [Full Text] [PDF]
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A. S. Kumar, S. Talwar, R. Mohapatra, A. Saxena, and R. Singh Aortic Valve Replacement With the Pulmonary Autograft: Mid-Term Results Ann. Thorac. Surg., August 1, 2005; 80(2): 488 - 494. [Abstract] [Full Text] [PDF]
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S.-P. Sommer, C. Bara, T. Kofidis, A. Haverich, and U. Klima Ross procedure with a quadricuspid pulmonary autograft J. Thorac. Cardiovasc. Surg., July 1, 2005; 130(1): 212 - 213. [Full Text] [PDF]
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= censored observations.
