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J Thorac Cardiovasc Surg 2007;134:90-98
© 2007 The American Association for Thoracic Surgery

Surgery for Congenital Heart Disease

Surgical strategy for the bicuspid aortic valve: Tricuspidization with cusp extension versus pulmonary autograft

^a Cardiac Surgery Unit, The Royal Children’s Hospital, Parkville, Victoria, Australia
^b Department of Pediatrics, The University of Melbourne, Melbourne, Victoria, Australia
^c Cardiovascular Surgery, Children’s National Medical Center, Washington, DC
^d Cardiology Department, The Royal Children’s Hospital, Parkville, Victoria, Australia.

Read at the Eighty-sixth Annual Meeting of The American Association for Thoracic Surgery, Philadelphia, Pa, April 29-May 3, 2006.

Received for publication May 4, 2006; revisions received January 2, 2007; accepted for publication January 8, 2007.

^_* Address for reprints: Christian Pierre Robert Brizard, MD, Cardiac Surgery Unit, The Royal Children’s Hospital, Flemington Rd, Parkville, Victoria, 3052, Australia. (Email: christian.brizard{at}rch.org.au).

	Abstract

Top Abstract Introduction Patients and Methods Results Discussion Limitations Conclusions Appendix References

 
Objective: The congenitally bicuspid aortic valve is the most common etiologic factor associated with clinically significant aortic stenosis and/or regurgitation in pediatric patients. Beyond infancy, surgical intervention typically involves valve repair with cusp thinning and commissurotomy or valve replacement, primarily with pulmonary autograft in the current era. An aortic valve repair technique using tricuspidization with cusp extension was introduced in 1999. This study compares the midterm clinical outcome in patients undergoing valve repair by tricuspidization with cusp extension with those receiving a pulmonary autograft (Ross).

Methods: A retrospective study was performed on all consecutive patients with symptomatic bicuspid aortic valve disease who underwent tricuspidization with cusp extension or a Ross procedure between 1999 and 2005. In both groups, all patients were at least 1 year of age at time of the operation.

Results: During this period, 21 children (median age 12.6 years, range 2.6–18 years) underwent tricuspidization with cusp extension (TCE group) and 25 children (median age 10.2 years, range 11.5 months–20.1 years) underwent the Ross procedure. Prior balloon valvuloplasty was performed in 5 (24%) of the children in the TCE group and 16 (64%) of the children in the Ross group. Prior surgical commissurotomy was performed in 4 (19%) TCE patients and in 9 (36%) Ross patients. During a median follow-up period of 36.4 months (range 2.5 months–7.4 years), 2 (10%) patients in the TCE group required valve-preserving early revision of the repair, 2 (10%) TCE patients required subsequent aortic valve replacement at 16 and 33 months, 1 (4%) Ross patient required subsequent valve repair at 5 years, and 1 (4%) Ross patient underwent cardiac transplantation at 46 months. At 36 months, the actuarial freedom from reintervention on the aortic valve or autograft was 90% in the TCE group, with 11 patients at risk, and 100% in Ross patients, with 13 patients at risk (P = .39); the freedom from moderate valve dysfunction or reintervention was 66% for TCE patients and 95% for Ross patients (P = .07). There were no deaths, and all but 1 Ross patient remain in New York Heart Association class I.

Conclusions: Reintervention rates in patients undergoing tricuspidization with cusp extension or a primary Ross procedure are similar. Valve performance in the TCE group is satisfactory at midterm follow-up, but the Ross repair appears to provide greater stability of valve function. These results suggest that repair with valve tricuspidization and cusp extension provides reliable palliation of the symptomatic bicuspid aortic valve.

	Introduction

Top Abstract Introduction Patients and Methods Results Discussion Limitations Conclusions Appendix References

 
Present in 1% to 2% of the population, the congenitally bicuspid aortic valve is the most common etiologic factor associated with clinically significant aortic valve stenosis in pediatric patients.¹ Critical bicuspid aortic stenosis is typically treated by balloon valvuloplasty or surgical valvotomy in neonates and infants. Beyond infancy, surgical interventions involve valve repair techniques or valve replacement, primarily using the pulmonary autograft (Ross procedure) in the current era. Although midterm results of the Ross procedure are encouraging,^2-4 there is evidence of increased valve dysfunction related to abnormal growth of the autograft in younger patients.^5,6 It has been reported that the pulmonary autograft is more prone to dysfunction in the setting of a predominantly regurgitant native aortic valve⁷ or significant size mismatch between the native valve and autograft. Additionally, it has been proposed that the presence of a native bicuspid aortic valve is an additional risk factor for pulmonary autograft dysfunction.⁸ Although early aortic valve repair is an attractive option in these patients, techniques that preserve bicuspid geometry are associated with increased risk of valve dysfunction and early valve replacement.⁹ The technique of bicuspid aortic valve repair by tricuspidization with cusp extension (TCE) was introduced in our unit in 1999. This study compares the midterm clinical outcome in children undergoing valve repair with TCE and those receiving a pulmonary autograft.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Discussion Limitations Conclusions Appendix References

 
From February 1999 to October 2005, 46 children (median age 13.3 years, range 11.5 months–20.1 years) underwent surgical treatment of congenitally bicuspid aortic valve disease at our institution. Indications for surgery were severe regurgitation or mean gradient greater than 50 mm Hg or a combination of mean gradient greater than 50 mm Hg and moderate regurgitation. Twenty-one of these patients (mean age 12.6 years, range 2.6–18 years) underwent aortic valve TCE and 25 patients (mean age 10.2 years, range 11.5 months–20.1 years) underwent placement of a pulmonary autograft (Table 1). The primary indication for surgery was aortic insufficiency in 11 (52%) TCE versus 5 (20%) Ross (P = .023), aortic stenosis in 1 (5%) TCE versus 2 (8%) Ross (P = .595), or combined aortic stenosis and insufficiency in 9 (43%) TCE versus 18 (72%) Ross patients (P = .044). The median preoperative z-value for the aortic valve annulus (at the nadir of the cusps) was +2.1 (range –0.3 to 9.2) in the TCE patients and +1.9 (range –4.4 to +8.7) in the Ross patients (P = .165). Moderate or greater preoperative aortic insufficiency was present in 16 (76.2%) TCE versus 21 (84%) Ross patients (P = .71), whereas moderate or greater aortic stenosis was present in 10 (48%) TCE and 10 (40%) Ross patients (P = .766). Balloon valvuloplasty had been previously performed on 5 (24%) TCE and 16 (64%) Ross patients (P = .007). Surgical commissurotomy had been performed on 4 (19%) TCE patients and 9 (36%) Ross patients (P = .173). Two (8%) Ross patients had previously undergone aortic valve repair. Precise anatomy and lesions are described in Table 2.

Surgical Technique
TCE
Through a full midline sternotomy, the anterior portion of the pericardium was exposed and carefully trimmed. A generous segment of pericardium was harvested before fixation in 0.625% glutaraldehyde for 8 minutes and rinsing.^12,13 When possible, pericardium overlying the superior cavoatrial junction was preferentially used because it is characteristically thin and supple.¹⁴ Cardiopulmonary bypass was performed with bicaval and ascending aortic cannulation. The aortic valve was exposed by a high transverse aortotomy (at least 1 cm above the anterior commissure) with extension deep into the noncoronary sinus (hockey-stick incision). Cold blood cardioplegic solution was given directly through the coronary ostia immediately after the aortotomy and then at 20-minute intervals. The cusps were then carefully examined and the annulus was measured with Hegar dilators. The raphe joining the congenitally fused cusps was divided to the aortic wall (Figure 1). When commissural fusion was present, commissurotomy was performed before determining the size of the annulus. Nodular irregularities along the surfaces of apposition of the cusps were removed.

View larger version (100K): [in this window] [in a new window]   Figure 1. A raphe joining two congenitally fused cusps is a common element of the bicuspid aortic valve. Division of the raphe to the aortic wall creates three functionally independent cusps before pericardial leaflet extension. Source: Brizard C, d’Udekem Y, Alphoso N, Valvar disease in children. In: Yuh D, Vricella L, Baumgartner W, eds. The Johns Hopkins Manual of Cardiothoracic Surgery. New York, NY: The McGraw-Hill Companies; 2007. p. 1301–28. Reprinted with permission of the publisher.

View larger version (87K): [in this window] [in a new window]   Figure 2. The height of coapting pericardial patches is increased toward the neocommissure to compensate for the lack of a true interleaflet triangle and to elevate the hinge point of the leaflets. Each new commissure is constructed by suturing the apposing short edges of each patch together and to the aortic wall, creating an elongated vertical axis of the native commissures. Source: Brizard C, d’Udekem Y, Alphoso N. Valvar disease in children. In: Yuh D, Vricella L, Baumgartner W, eds. The Johns Hopkins Manual of Cardiothoracic Surgery. New York, NY: The McGraw-Hill Companies; 2007. p. 1301–28. Reprinted with permission of the publisher.

Follow-up
All patients underwent transthoracic echocardiographic examination before hospital discharge and then usually at 6-month intervals unless a change in clinical examination or status was noted. Mean patient follow-up for the series was 36.4 months (range 2.5 months–7.4 years). Follow-up data were complete for all patients.

Statistical Methods
Statistical analysis was performed with Stata Version 8 software (StataCorp LP, College Station, Tex). Mean and sample proportions are expressed with 95% confidence limits (CL), using continuity correction for the upper and lower limits. Groups were compared by unpaired t tests for continuous variables or Fisher exact tests for dichotomous variables. Survival analysis was performed by the Kaplan–Meier method and comparison of survival curves was performed by the log–rank test. Univariate analysis with logistic regression was used to test risk factors for failure. This study was done within the guidelines established by our institutional human research ethics committee.

	Results

Top Abstract Introduction Patients and Methods Results Discussion Limitations Conclusions Appendix References

 
TCE
TCE was performed in all patients who fulfilled the selection criteria described in the "Patients and Methods" section. Two patients required early revision of the repair—during the same operation for one and on the second postoperative day for the other. The native valve was preserved in both patients; one required pericardial extension replacement with higher patches, and the other needed a small triangular resection at the center of one of the patches. Postoperative echocardiography demonstrated a peak outflow tract gradient greater than 20 mm Hg in 3 patients (22, 22, and 27 mm Hg). Residual aortic regurgitation at hospital discharge and at latest follow-up is presented in Figure 3. During a median follow-up of 34.7 months (range 8 months-6.5 years), 1 patient underwent a Ross procedure for endocarditis 16 months after TCE and 1 patient required bioprosthetic aortic valve replacement for progressive aortic insufficiency 33 months after repair (9.5%, CL: 0.1-32). In 4 patients a moderate aortic regurgitation was first diagnosed 9, 10, 31, and 40 months, respectively, after the TCE; severe regurgitation did not develop in any patient (Figure 3). At latest follow-up, the median peak instantaneous Doppler gradient was 20 mm Hg (range 10-55 mm Hg) with 6 peak gradients greater than 20 mm Hg (23 mm Hg, n = 3; 30 mm Hg first noted at 38 months, 36 mm Hg first noted at 26 months, and 55 mm Hg first noted at 30 months). All patients are in New York Heart Association class I.

View larger version (19K): [in this window] [in a new window]   Figure 3. The degree of residual aortic regurgitation at the time of hospital discharge (upper panels) and at latest follow-up (lower panels) in patients undergoing tricuspidization with leaflet extension (TCE, left panels) and pulmonary autograft (Ross, right panels). TCE, Tricuspidization with cusp extension.

During this time, 2 (8%, CL: 1.3-27) Ross patients required surgical or catheter-based intervention for right ventricle–pulmonary artery conduit failure.

Statistical Analysis
Two (10%) TCE and 6 (25%) Ross patients were free of aortic insufficiency (P = .26) at latest follow-up. The degree of aortic regurgitation at discharge was similar between the two groups (P = .06) but significantly different at latest follow-up (P = .027). The degree of regurgitation increased significantly for the TCE patients (P = .035), whereas it did not for the Ross patients (P = .24). The actuarial freedom from aortic valve reoperation was comparable between the two groups (log–rank test, P = .39) (Figure 4). The actuarial freedom from moderate or greater aortic regurgitation or reoperation (excluding right ventricular outflow tract procedures and cardiac transplantation) was also comparable between the two groups (log–rank test, P = .075) (Figure 5).

View larger version (8K): [in this window] [in a new window]   Figure 4. Kaplan–Meier curve comparing freedom from surgical reintervention on the aortic valve in patients undergoing pulmonary autograft (Ross, solid lines) and those undergoing tricuspidization with leaflet extension (TCE, dashed lines). Freedom from surgical reintervention at 36 months was 100% for Ross patients (13 patients at risk) and 90% for TCE patients (11 patients at risk) (P = .39). TCE, Tricuspidization with cusp extension.

View larger version (9K): [in this window] [in a new window]   Figure 5. Kaplan–Meier curve comparing freedom from reoperation or the development of moderate or greater aortic regurgitation in patients undergoing pulmonary autograft (Ross, solid lines) and those undergoing tricuspidization with leaflet extension (TCE, dashed lines). Freedom from reoperation or moderate or greater aortic regurgitation at 36 months was 90% for Ross patients (13 patients at risk) and 75% for TCE patients (10 patients at risk) (P = .075). TCE, Tricuspidization with cusp extension.

Multivariate logistic regression was also performed with valve dysfunction or occurrence of reoperation as the dependent variable whereas the independent variables included the type of operation (TCE or Ross), age, body surface area, prior surgical intervention, mean valve gradient before, the dominant preoperative valve disease, and the grade of the preoperative valve regurgitation. There were no significant predictive variables.

Cox proportional analysis was performed, with time to reoperation used as the dependent variable. There were no significant predictive variables.

	Discussion

Top Abstract Introduction Patients and Methods Results Discussion Limitations Conclusions Appendix References

 
Introduced by Ross¹⁶ in 1967, the pulmonary autograft has become an important therapeutic option for patients with severe aortic valve disease. In the young adult population, the pulmonary autograft has proven to be a practical alternative to prosthetic aortic valve replacement, with reported freedom from reoperation of 75% at 10 years¹⁷ on the autograft. However, additional procedures are necessary to address subsequent right ventricle–pulmonary conduit dysfunction. A major drawback of the Ross procedure is that the patient is converted from single-valve disease to iatrogenic 2-valve disease.

Surgical repair of the congenitally bicuspid aortic valve is an attractive alternative to valve replacement. Valve repair preserves the native aortic root and, therefore, enables normal annular growth to occur. This is an important consideration in the younger child whose aortic annulus will not accommodate an adult-sized prosthesis. The goal of aortic valve repair in these patients is to prevent secondary changes in left ventricular geometry and function and to facilitate sufficient annular growth to accommodate an aortic valve prosthesis when necessary. Furthermore, aortic valve repair preserves the pulmonary valve and does not preclude a subsequent pulmonary autograft.¹⁸ Conversely, the results of bicuspid aortic valve repair in children are frequently not encouraging, with some groups reporting that approximately 50% of patients will require valve replacement or exhibit significant valve dysfunction within 2 years.⁹

Several surgical techniques involving valve reconstruction with autologous tissue have been developed since Senning’s initial report¹⁹ on the use of fascia lata to reconstruct the aortic valve in 1967. Although some authors discourage the use of cusp extension for aortic insufficiency in children,²⁰ experience with autologous pericardial cusp extension techniques for rheumatic aortic valve repair has demonstrated reasonable midterm durability in both adults and children.^21-23 Early²⁴ and midterm²¹ results of cusp extension techniques to address bicuspid valve dysfunction are also encouraging. Using univariate analysis, van Son and colleagues⁹ identified the presence of a bicuspid aortic valve as an independent risk factor for early repair failure. When compared with cusp extension for bicuspid aortic valve disease, valve repair involving tricuspidization with cusp extension (TCE) appears to offer improved durability, albeit not statistically significantly so.²¹

Surgical repair of the bicuspid aortic valve must frequently address both residual stenosis and insufficiency, which may or may not be related to prior balloon dilation. We believe that it is critical not only to increase the cusp zone of apposition but also to establish tricuspid geometry to provide an optimal effective orifice area. Balloon valvuloplasty during childhood tends to disrupt valves along planes of least resistance, causing damage to delicate cusp tissue, which leads to valvular insufficiency.²⁵ Balloon valvuloplasty had been performed in only 24% of patients eligible for TCE in this series, whereas 64% of patients who were not TCE candidates had undergone previous balloon valvuloplasty. It may be beneficial to consider surgical valvotomy, rather than balloon valvuloplasty, in infants with critical bicuspid aortic stenosis and an adequate aortic annulus.

Before the introduction of the Ross procedure, the surgical strategy for congenital aortic valve disease at The Royal Children’s Hospital was to delay valve replacement by performing palliative valve repairs until an adult-sized mechanical prosthesis could be used.²⁶ The cusp extension technique for bicuspid aortic insufficiency was introduced in our unit at the same time as the Ross procedure. From 1996 to 1999, we performed cusp extensions, preserving bicuspid anatomy. The results in these early patients were disappointing, with excessive residual gradients and early failure owing to recurrent regurgitation (Appendix Figure 1). The technique of TCE was introduced in 1999. It is derived from valve tricuspidization, as promoted by Tolan and associates,²⁷ and cusp extension, first described by Senning.¹⁹

View larger version (8K): [in this window] [in a new window]   Appendix Figure 1 Actuarial freedom from reoperation for aortic valve repair for bicuspid aortic valve (Royal Children’s Hospital, 1996-1998) with preservation of the bicuspid physiology. N = 5. The only patient of the 5 with a long-term satisfactory result has not had a cusp extension with pericardium. The other 4 had cusp extension.

Over the time of the follow-up, the two groups had comparable reoperation rates; however, it is clear that aortic valve function in TCE patients is less stable than in Ross patients. Identification of risk factors contributing to TCE failure would clearly be beneficial for future patient selection, but we failed to detect any significant factors. The fact that we were unable to identify risk factors for TCE or Ross failure may suggest that our choice of procedure at the time of surgery was appropriate or that the power of the study is limited owing to the small number of events and/or patients. Patients at risk for failure with one procedure were directed toward the alternate procedure. Although not statistically significant, younger age at time of operation was associated with subsequent development of aortic insufficiency in TCE patients. This is disappointing inasmuch as limiting TCE to older patients defeats the primary benefit of valve repair in children, which is to delay valve replacement as long as possible.

Although early valve function after TCE is excellent, the results from this series and others^21,29 suggest that long-term follow-up will be associated with an increased rate of reoperation. The importance of the characteristics of the material used for cusp extension in the long-term result is obvious and, therefore, the selection of material is essential. We belong to a school that has extensively studied and promoted the use of glutaraldehyde-treated autologous pericardium.^{12,13,22,30,31} We harvest the thinnest portion of the pericardium and carefully clear it of any scar tissue. We have reduced the duration of the treatment to 8 minutes. However, other materials have been used and advocated by other teams. Most centers now avoid using glutaraldehyde-treated bovine³² or equine pericardium. There is one case report describing the use of dye-mediated photo-oxidation bovine³³ pericardium in this context without cusp extension but without follow-up. Kalangos and associates³⁴ also report good midterm results with the use of untreated autologous pericardium for rheumatic aortic valve repair. Similar reports by Grinda and colleagues²³ and others²² with large series yield good midterm results as well for the cusp extension with glutaraldehyde-treated pericardium. Although thin expanded polytetrafluoroethylene appears to provide satisfactory function during early follow-up in the pulmonary position, this material is likely to tear at systemic pressure and its use in the systemic circulation has not been reported. In this context, and although the results are imperfect, there is no strong argument to justify for us a switch to an alternative material. Most teams involved with this operation would agree that the ideal material for aortic valve repair is still to be found.

The TCE is particularly well suited for the thickened cusps seen in pediatric patients with a history of valve stenosis or when significant secondary dysplasia contributes to increased valve gradient. However, it must be noted that other repair techniques exist for bicuspid aortic valve disease. In the setting of a bicuspid valve with thin cusps, symmetrical commissures without raphe and elongation of one free edge, triangular resection of the free edge without cusp extension is a very efficient repair technique.^35,36 These patients often first present in the second or third decade and are rare in pediatrics settings.

	Limitations

Top Abstract Introduction Patients and Methods Results Discussion Limitations Conclusions Appendix References

 
We recognize that this is a nonrandomized retrospective series. The patients are essentially different, because the two techniques address and are best suited for dissimilar valve anatomy. Therefore, the statistical comparison between the two groups should be interpreted carefully and more as an indication of the midterm performance of the TCE benchmarking with the Ross procedure.

	Conclusions

Top Abstract Introduction Patients and Methods Results Discussion Limitations Conclusions Appendix References

 
This series demonstrates that TCE is a reliable palliation for symptomatic bicuspid aortic valve disease beyond infancy and is associated with very little morbidity. TCE should not be viewed as an alternative to the pulmonary autograft, which has very good midterm results. When integrated into a comprehensive surgical strategy, TCE may delay the timing of the Ross procedure or other aortic valve replacement while preserving ventricular function, especially in patients less suited for pulmonary autograft.

	Appendix

Top Abstract Introduction Patients and Methods Results Discussion Limitations Conclusions Appendix References

 

	References

Top Abstract Introduction Patients and Methods Results Discussion Limitations Conclusions Appendix References

 

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