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Eur J Cardiothorac Surg 2008;34:583-588. doi:10.1016/j.ejcts.2008.05.056
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.

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Long-term follow-up of supra-annular pulmonary autograft aortic root replacement in patients with bicuspid aortic valve

Feyzan Özaslana,*, Thomas Wittlingera, Nadejna Monsefia, Tamimount Bouhmidia, Sinthu Theresa, Mirko Dossa, Gerhard Wimmer-Greineckerb, Anton Moritza

a Department of Thoracic & Cardiovascular Surgery, Johann Wolfgang Goethe University Hospital, Frankfurt-Main, Germany
b Cardio-Vascular Centre, Bad Bevensen, Germany

Received 9 October 2007; received in revised form 6 May 2008; accepted 9 May 2008.

* Corresponding author. Address: Department of Thoracic & Cardiovascular Surgery, Johann Wolfgang Goethe University Hospital, Theodor-Stern-Kai 7, 60596 Frankfurt-Main, Germany. Tel.: +49 69 6301 6141; fax: +49 69 6301 5849. (Email: dr.feyzanoezaslan{at}o2online.de).


    Abstract
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Objective: The performance of the Ross procedure in the case of geometric mismatch between pulmonary autograft and a bicuspid aortic root has not yet been fully evaluated. To prevent geometrically caused autograft dysfunction, a modification of the surgical technique is necessary. Methods: Between January 1996 and January 2007, 50 patients (33 male, 17 female; mean age 50 ± 14 years; range 13–63 years) underwent replacement of a diseased bicuspid aortic valve (stenosis in 14 cases; insufficiency in 21; combined disease in 15) with a Ross procedure. The pulmonary autograft was inserted partially in supra-annular position to correct the geometric mismatch between the deeper base of the non-coronary sinus and the right/left coronary sinus. In 24 of these patients, additional tailoring of the non-coronary sinus was necessary. In eight patients the non-coronary sinus was covered with a glutaraldehyde treated autologous pericardial patch to prevent pseudoaneurysm formation. Patients were followed up 1, 2, 5 and 10 years postoperatively. Results: There were no early or late deaths. There were six reoperations. One patient was reoperated because of persistent severe aortic valve insufficiency 9 months postoperatively. Three patients were reoperated for formation of subannular pseudoaneurysm, 6, 9 and 30 months postoperatively. One patient was reoperated for closure of a paravalvular dehiscence. Another patient was reoperated 1 year postoperatively because of a severe pulmonary stenosis due to excessive calcification of the bioprosthesis. Echocardiographic follow-up of the remaining patients showed no evidence of residual or recurrent pulmonary autograft regurgitation or progression of aortic root dilatation. Conclusion: Autograft replacement of the bicuspid aortic valve is challenging, as the geometric mismatch has to be adjusted. Valve dysfunction is avoided by a supra-annular implantation technique, but pseudoaneurysm formation at the base of the non-coronary sinus is a worrying aspect. Patch reinforcement may solve this issue.

Key Words: Bicuspid aortic valve • Ross procedure • Aortic valve replacement


    1. Introduction
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Bicuspid aortic valve (BAV) is considered the most common congenital heart defect with a generally accepted prevalence rate of 1–2% [1]. BAV is mostly associated with clinically significant aortic stenosis and/or regurgitation [2]. Currently replacement of the aortic valve or aortic root with a pulmonary autograft is a frequently used technique for the treatment of BAV [3]. The procedure offers many theoretical advantages including low preoperative mortality, excellent hemodynamic performance, extreme low prevalence of infection and no need for anticoagulation [1]. However, the need for reoperation remains a principal limitation of the procedure. When root replacement is used, progressive dilatation of the autograft with or without regurgitation of the neo-aortic valve is a common indication for reoperation [4].

Subcoronary implantation may be challenging in the case of geometric mismatch between the bicuspid root and the tricuspid autograft. Most frequently the right- and left-coronary cusps are fused. Then the base of the non-coronary sinus is positioned deeper in the left ventricular outflow tract than the others. In addition the annulus may be wider and the position of the true commissures varies between a 120° and a 180° graduation. To prevent immediate and progressive valve dysfunction, a modification of the full root technique is necessary in order to adjust for the differences and achieve a primarily competent valve.

The objective of this prospective study was to evaluate mid-term and long-term clinical and echocardiographic outcome of a series of 50 patients with BAV replaced by the pulmonary autograft in modified full root technique.


    2. Material and methods
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
2.1 Patient population
Between January 1996 and January 2007, 50 patients underwent replacement of a diseased bicuspid aortic valve (stenosis in 14 cases; insufficiency in 21 cases; combined disease in 15) using a Ross procedure with the root replacement technique. The patients ranged in age from 13 to 63 years old (mean 50 ± 14 years old) and 33 (66%) were male. Ten of these patients also had aneurysms of the ascending aorta, in nine patients a reduction plasty of the ascending aorta was performed and in one patient the ascending aorta was replaced with a Dacron graft.

Preoperatively, the majority of the patients were in NYHA functional class two to three. Table 1 demonstrates the patient characteristics.


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Table 1 Patient characteristics
 
2.2 Operative procedure
The aortic root replacement with a pulmonary autograft has been previously reported by other groups [1–4]. The technique to adjust for diameter and partition mismatch has been described before [5]. Additionally we have inserted the pulmonary autograft in a partial supra-annular position to correct for the geometric mismatch between the base of non-coronary sinus and the right or left coronary sinus respectively (operative technique I, Fig. 1 ). By doing this, the base of the three autograft bases remained in their anatomic plane. In 24 patients, additional tailoring of the non-coronary sinus was performed to compensate for the sinus bulge, which adds to the new annulus diameter (operative technique IIa, Figs. 2–3 ). The non-coronary sinus was reinforced with an autologous pericardial patch to prevent pseudoaneurysm formation after debridement of calcium later in the series (operative technique IIb, Fig. 4 ). The coronary arteries were re-implanted as buttons. After mobilization it was always possible to reimplant them without tension, however sometimes asymmetrically in the autograft root. The autograft root was reinforced with the remnants of the aortic root. The tips of the original commissures were sutured to corresponding adventitia of autograft or aorta respectively. An additional Vicryl (Ethicon, Norderstedt, Germany) or Vypro (Ethicon, Norderstedt, Germany) mesh was used to prevent aortic root dilatation. The mesh was fixed with two stitches at the base of the noncoronary sinus, and then it was flipped around the aorta and adapted ventrally with slight tension. Thus mesh and aortic wall remnants prevented dilatation of the neo aortic root. Care was taken to avoid any ostia constriction; the small area beneath the coronary ostia was not covered.


Figure 1
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Fig. 1. Surgical anatomy of aortic valve for Ross procedure.

 

Figure 2
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Fig. 2. Triangular resection of aortic annulus in case of dilatation.

 

Figure 3
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Fig. 3. Reduction of diameter of aortic annulus has been performed.

 

Figure 4
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Fig. 4. Reinforcement of the non-coronary sinus a glutaraldehyde treated autologous pericardial patch to prevent pseudoaneurysm.

 
Intraoperative transesophageal two-dimensional and color flow Doppler transesophageal echocardiography (TEE) was performed in all patients to measure the diameter of the aortic and 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 Toronto SPV sizer.

The right ventricular outflow tract was replaced with a pulmonary homograft in 40 patients and with stentless bioprostheses (Freestyle, Medtronic Inc., USA) in 10 patients. The homografts were not matched to the blood group of the patient.

The duration of cardiopulmonary bypass was 164 ± 23 min. During the period of myocardial ischemia, which was 109 ± 20 min, the myocardium was protected by intermittent infusion of a cold blood cardioplegia solution directly into the coronary ostia or retrograde into the coronary sinus. After discontinuation of cardiopulmonary bypass, the competence of the pulmonary autograft valve and the pulmonary homograft valve in the right ventricular outflow tract was assessed by TEE.

2.3 Associated procedures
In addition, one patient had replacement of the ascending aorta, one had repair of the mitral valve, and three patients had coronary artery bypass grafting.

In nine patients the dilated aorta was reduced in diameter and adjusted to the autograft sinotubular junction by longitudinal excision of excess wall and reanastomosing with a running mattress and secondly an over and over 4/0 Prolene suture line.

2.4 Postoperative evaluation and management
Transthoracic M-mode, two-dimensional, color-flow, and Doppler echocardiograms were obtained before discharge from the hospital and at 6–12 month intervals thereafter. The severity of neo-aortic valve regurgitation (AR) was measured using a modification of the method of Perry and colleagues [6], 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 peak velocity of flow across the pulmonary autograft and pulmonary homograft valves was also measured, and gradients were estimated using the modified Bernoulli equation. The echocardiograms were interpreted by two cardiologists and two cardiac surgeons. Serial echocardiography studies in all patients were suitable for analysis.

No oral anticoagulants were administered to the patients after operation. Use of platelet anti-aggregating agents in the follow-up period was left to the discretion of the attending cardiologist. The mean duration of follow-up was 6.2 years.

2.5 Statistical analysis
All statistical analyses were performed with the StatView program (Carry, NC, USA). Continuous variables are expressed as mean ± standard deviation and were evaluated by Student's t-test. Statistical significance was defined as a p value less than 0.05.


    3. Results
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Table 2 demonstrates the preoperative results. Four patients (8%) required reoperation for bleeding postoperatively. Ventricular dysrhythmias requiring drug therapy occurred in two patients (4%). No patient required implantation of a permanent pacemaker. Two patients had temporary low output syndrome with need of inotropic support (4%). One patient developed a temporary partial homonymous hemianopsia (2%). The postoperative length of stay in the hospital was 8 ± 4 days.


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Table 2 Perioperative results and surgical procedures
 
No other patient sustained a postoperative embolic event. There was no early or late death. The 10-year actuarial survival was 100%.

The actuarial freedom from thromboembolism at 10 years was 98%. Two patients developed endocarditis of the pulmonary autograft developing a paravalvular leak. A complex pericardial reconstruction with repair of the autograft resolved the problem and maintains the pulmonary autograft competence.

One patient developed a severe pulmonary stenosis due to excessive calcification of the bioprosthesis 1 year postoperatively. He underwent successful replacement elsewhere.

3.1 Reoperation
There were six reoperations. Five patients required reoperation on the pulmonary autograft. One patient was reoperated because of persistent severe aortic valve insufficiency 9 months postoperatively. Three patients were reoperated for formation of subannular pseudoaneurysm 9–30 months postoperatively with competent valves.

Decalcification of the non-coronary annulus was performed in these patients. At reoperation we found a pseudoaneurysm beneath the noncoronary sinus. The entrance was partially calcified in two cases so that it was not possible to discern whether the cause was degeneration or healed endocarditis. The patients underwent resection of the pseudoaneurysm if possible and subsequent reconstruction by closure of the entrance with a pericardial patch and commissural plication.

One patient was reoperated for closure of a paravalvular dehiscence after endocarditis. This patient had undergone perioperative reexploration for bleeding. As observed at reoperation, one of the sutures placed for hemostasis had caught one of the commissures, and thus caused severe regurgitation. In addition, the aortic wrap and the Vicryl reinforcement had been removed. Rerepair by annuloplasty with an initially successful result was performed. However, dilatation of the aortic root progressed and the patient was scheduled for mechanical aortic valve replacement 1 year later.

Another patient was reoperated 1 year postoperatively because of a severe pulmonary stenosis due to endocarditis of the bioprosthesis.

All patients survived reoperation and were all alive at the date of last follow-up.

Event-free survival (freedom from death, reoperation, thromboembolism, and endocarditis) was 84% at 10 years postoperatively. Table 2 summarizes the perioperative and postoperative complications.

3.2 Echocardiographic studies
The postoperative aortic regurgitation was mild (grade I–II) in two cases (4%) and less than trivial in all other cases. Progression of aortic regurgitation occurred in the one patient mentioned above. They had trivial central regurgitation postoperatively that increased to grade II regurgitation at 2 and 5 years, respectively and was stable thereafter. The patients remain under close observation. The echocardiographic outcomes of the pulmonary autograft are listed in Table 3 . Table 4 contains all postoperative measurements of autograft diameters.


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Table 3 Echocardiographic outcome
 

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Table 4 Postoperative echocardiographic measurements of autograft diameters
 

    4. Discussion
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Over the past three decades, extensive experience has accumulated with the use of pulmonary autografts for replacement of the aortic valve and the aortic root. Three general techniques for insertion have been used: subcoronary valve implantation, mini root implantation and full root replacement [7].

There has been a trend in many centres towards exclusive use of the root replacement technique. This technique preserves the anatomical unit of the pulmonary root and may reduce the potential risk of incorrect anatomical positioning. Reoperation for regurgitation of the pulmonary autograft is the major complication of the Ross procedure [8]. In the pioneering series of Ross freedom from reoperation was 76% at 10 years and 62% at 20 years [2,8]. Geometric mismatch between the patients’ two semilunar valves has been identified as a risk factor for the incidence of pulmonary autograft regurgitation [9]. Therefore, tailoring of the aortic root by reduction annuloplasty of the aortic annulus and the sinotubular junction has been introduced [9,10]. Surgical adjustment of the aortic root diameter at the level of the annulus and the sinotubular junction to match the autograft resulted in a significantly reduced incidence of regurgitation, with mild to moderate incompetence rates of 4–10% at 5 years [9,11]. Patients with bicuspid aortic valve disease have been treated with the Ross procedure by several groups [9,12]. Congenital bicuspid aortic valve disease is the most common aortic valve pathology in young patients with an incidence of 1–2%. It is commonly associated with dilatation of the aortic root [13]. Furthermore, the aortic root in most of the patients is asymmetric, the acoronary sinus is usually larger than the coronary sinus and the line of insertion of the noncoronary leaflet is displaced below that of the coronary leaflet. Thus, the base of the noncoronary leaflet lies below that of the coronary leaflets. Any attempts to suture the normal pulmonary autograft into the annulus of the native bicuspid aortic valve will therefore cause distortion of the pulmonary valve geometry and subsequent incorrect leaflet apposition, leading to decreased coaptation surface, increased stress on the leaflets and eventually to valve incompetence. Tailoring of the aortic annulus and sinotubular junction are inadequate measures, in this case, to overcome geometric mismatch. Therefore, we decided to modify our implantation technique, to tackle the challenges posed by the asymmetric sinuses and different heights of leaflets insertion. As described in the methods section, this meant implanting part of the autograft higher into the wall of the noncoronary sinus, after surgically reducing its diameter to match that of the pulmonary valve, in some cases. Thus, the base of the pulmonary autograft is in one plane and distortion of valve geometry is avoided. Five of our patients required reoperation on the pulmonary autograft. One due to progressive aortic root dilatation and three due to development of subaortic pseudoaneurysms, one to a ‘paravalvular’ dehiscence.

Dilatation of the pulmonary root after transfer to the aortic position has been described in literature and remains a cause of concern after the Ross procedure [4]. As in pulmonary hypertension and after arterial switch operations the pulmonary wall tends to dilate late when exposed to systemic pressures. We thus reinforced the neo aortic root with aortic wall remnants with resorbable mesh. In one of our patients in whom the protective wrap was removed at reoperation for hemostasis late aortic dilatation and valve incompetence developed.

The development of pseudoaneurysm after the Ross procedure may be caused by several factors. From the experience with the Cryolife-O’Brian (Cryolife International, Atlanta, GA) stentless bioprosthesis, which is implanted in a supra-annular position, we have learned that suturing a prosthesis into the supra-annular position is safe. However, some authors describe the event of posterior atrioventricular bleeding after supra-annular stentless aortic valve replacement [14]. They conclude that radical debridement of valve leaflets and aortic annulus may weaken the aortic wall below the suture line of the bioprosthesis, which is in turn exposed to ventricular pressures upon resumption of cardiac activity. Therefore, they advocate pre-emptive reinforcement of the aortic root.

There is evidence that an aortopathy may be present or may develop in patients with bicuspid aortic valve disease [15]. Second, examination of the histological features of the ascending aorta and the main pulmonary artery in patients with bicuspid aortic valve disease, showed an increased incidence of changes in smooth muscle cell orientation, elastic fragmentation and cystic media necrosis in both the ascending aorta and the pulmonary trunk, rendering these patients at a higher risk for aortic root dilatation, type A dissection and pseudoaneurysm formation [16]. Part of this potentially weakened aortic wall is exposed to ventricular pressures by the described technique.

The first reoperated patient was the only one in our whole series who had a prosthetic interposition to repair his concomitant ascending aortic aneurysm. At the initial revision for bleeding one stitch caught a commissure and the autograft wall reinforcement was removed. Even short segments of prostheses increase the pressure velocity downstream [17]. A progressive aortic incompetence developed but was deemed amenable for repair. This finally failed due to progressive dilatation, underscoring the importance of our policy of neo-aortic wall reinforcement.

Many groups tend to replace the ascending aorta prophylactically with replacement of a bicuspid valve due to inherent wall pathology. However, we and others did not observe redilatation of an ascending aorta after cure of the valve defect once a normal diameter of the aorta has been achieved by a reduction plasty [18]. We rarely performed a Ross procedure in patients with extensive aneurysms primarily for the fact that the autograft upstream to a stiff vascular prostheses exposed it to higher mechanical stress.

The causes for the subaortic pseudoaneurysms were difficult to identify. At reoperation we found the aortic wall at the entrance to the aneurysm thickened and calcified. This may be an indication for endocarditis as etiology. All patients had calcified aortic stenoses as primary indication. After debridement a weakened aortic ring remained thus in the subaortic position and may have been the cause for progressive expansion. Healing may well be different along a suture line of a resected leaflet than to a relatively intact aortic wall. In the following cases we thus reinforced the noncoronary base with a strip of autologous pericardium. The reoperation rate of the reported group is much higher than in our total group of autografts, where we observed 11 reoperations out of 143 patients. In the contemporary literature freedom from reoperation after the Ross procedure range between 90% and 94% after 8 years [19,20].

Five reoperations were due to problems of the autograft; all were initially re-repaired. Three patients of the whole group finally underwent mechanical aortic valve replacement. At latest follow-up, 4% of the patients (2/50) had mild (grade II) pulmonary autograft regurgitation. This is comparable to the mid-term results reported by other authors for the replacement of bicuspid aortic valves, with pulmonary autografts [3,8]. In conclusion, the Ross procedure is a safe and effective way to treat patients with bicuspid aortic valve disease. Adaptation of the asymmetric aortic root to the symmetry of the autograft is important to achieve primary competence and stress free valve action. Reoperation for development of pseudoaneurysms is a major complication and stresses the importance of reinforcement of the subaortic annular wall remnants after ring decalcification.


    Appendix A
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Conference discussion

Dr J. Pepper (London, United Kingdom): It is an interesting approach to put this in a supra-annular position, but if you put the valve down into the left ventricular outflow tract, you could solve the problem in the other way and you would also protect the thin wall of the pulmonary autograft root, making it less likely to dilate. So you decided to go up but you could have gone down, as one sometimes has to do in endocarditis.

Dr Özaslan: You have a better horizontal position if you put it in the upper supra-annular position I think.

Dr G. Ziemer (Tuebingen, Germany): Although your primary topic was the root and the annulus size, however, we all know that with bicuspid aortic valves there is a very high incidence of late ascending aortic aneurysm. And the way you treat it now, these obviously already to some amount dilated ascending aortas, this would mean that nowadays we can deal in ascending aortic aneurysm or ectasia just with a reduction plasty, which is not true. So I assume that in these patients with some longer follow-up you will still see ascending aortic aneurysms, and that is why now in bicuspid aortic valve disease which requires valve replacement we rather would do a homograft instead of these autografts, although we have not seen this problem yet.

Dr Özaslan: In this group in one person the ascending aorta was wide, so we had to put a prosthesis in it, but the other patients had only ectases, so we can reduce this with a reduction plasty and put a mesh around the root and part of the ascending aorta, and that reinforces this area in our follow-up.

Dr Zeimer: Considering the mean age of your patient group and the mean follow-up I think you will see this problem.

Dr Özaslan: Maybe.


    Footnotes
 
{star} Presented at the 21st Annual Meeting of the European Association for Cardio-thoracic Surgery, Geneva, Switzerland, September 16–19, 2007.


    References
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A
 References
 

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  11. Svensson G, Aljassim O, Svensson SE, Bech-Hanssen O, Kjellman U. Anatomical mismatch of the pulmonary autograft in the aortic root may be the cause of early aortic insufficiency after the Ross procedure. Eur J Cardiothorac Surg 2002;21:1049-1054.[Abstract/Free Full Text]
  12. Schmidtke C, Bechtel M, Hueppe M, Sievers HH. Time course of aortic valve function and root dimensions after subcoronary Ross procedure for bicuspid versus tricuspid aortic valve disease. Circulation 2001;104:I21-I24.[Medline]
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  14. Mediratta N, Sosnowski AW, Galinanes M. Posterior aortoventricular bleeding after supra-annular stentless aortic valve replacement. J Thorac Cardiovasc Surg 1999;117:1031-1032.[Free Full Text]
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