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The utility of aortic valve leaflet reconstruction techniques in children and young adults

Open ArchivePublished:October 26, 2019DOI:https://doi.org/10.1016/j.jtcvs.2019.09.176

      Abstract

      Objectives

      The treatment of aortic valve disease in children and adolescents requires an individualized approach to provide a long-term solution with optimal hemodynamic profile. The role of aortic leaflet reconstruction techniques is evolving.

      Methods

      We retrospectively reviewed the charts of 58 patients who underwent aortic valve tricuspidalization either by an Ozaki procedure (neo-tricuspidalization) or single leaflet reconstruction between 2015 and 2019. Immediate operative results as well as hospital and short-term outpatient follow-up data were evaluated.

      Results

      Fifty-eight patients underwent leaflet reconstruction with 40 (69%) receiving a neo-tricuspidalization and 18 patients (31%) undergoing single leaflet reconstruction, using either a glutaraldehyde fixed autologous pericardium or tissue engineered bovine pericardium (CardioCel; Admedus, Queensland, Australia). The median age at the time of surgery was 14.8 years (interquartile range, 10.6-16.8 years). Twenty-three patients (40%) had isolated aortic regurgitation. The peak velocity across the aortic valve decreased from 3.4 ± 1.2 meters per second (m/s) preoperatively to 2.0 ± 0.4 m/s (P < .001) after surgery and remained stable (2.2 ± 0.7 m/s) during a median echocardiographic follow-up of 14.1 months (7.2-20.1 months) for the whole cohort. Freedom from reoperation or moderate and greater aortic regurgitation at 1, 2, and 3 years was 94.2% ± 3.3%, 85.0% ± 5.8%, and 79.0% ± 8.0%, respectively, with no difference between the neo-tricuspidalization and single leaflet reconstruction groups (P = .635). There were 6 late reoperations (10%) of which 3 were due to endocarditis.

      Conclusions

      Aortic leaflet reconstruction provides acceptable short-term hemodynamic outcomes and proves the utility of this technique as an adjunctive strategy for surgical treatment of aortic valve disease in children and young adults.

      Key Words

      Abbreviations and Acronyms:

      AR (aortic regurgitation), SLR (single leaflet reconstruction)
      Figure thumbnail fx1
      Box plots depicting peak aortic valve velocities preoperatively, immediately postoperatively, and at follow-up for the entire cohort.
      Aortic leaflet reconstruction techniques may offer a valuable alternative in children and young adults with aortic valve disease.
      Aortic leaflet reconstruction techniques can be applied in children and young adults with acceptable immediate hemodynamic outcomes. These short-term outcomes must be weighed against the need for late reoperation after the Ross procedure, disappointing long-terms result of various aortic valve repair techniques, and important anticoagulation related morbidity following mechanical valve replacement.
      See Commentaries on pages 2379, 2380, and 2381.
      Children and young adults with aortic valve disease continue to present a challenging pathology to manage. They require an individualized treatment approach based on the aortic valve anatomy, associated cardiac lesions, previous valve interventions, patient size and age at the time of intervention, as well as surgeon experience. The management strategy pursued must consider the durability provided to minimize the need for repetitive procedures, as well as the morbidity associated with lifelong anticoagulation therapy.
      Balloon valvotomy or open surgical valvotomy are used as the initial intervention in neonates and children with aortic valve stenosis, but regardless of initial strategy many require further surgical intervention within 10 years.
      • Pedra C.A.
      • Sidhu R.
      • McCrindle B.W.
      • Nykanen D.G.
      • Justo R.N.
      • Freedom R.M.
      • et al.
      Outcomes after balloon dilation of congenital aortic stenosis in children and adolescents.
      • d'Udekem Y.
      • Siddiqui J.
      • Seaman C.S.
      • Konstantinov I.E.
      • Galati J.C.
      • Cheung M.M.
      • et al.
      Long-term results of a strategy of aortic valve repair in the pediatric population.
      • Brown D.W.
      • Dipilatp A.E.
      • Chong E.C.
      • Lock J.E.
      • McElhinney D.B.
      Aortic valve reinterventions after balloon valvuloplasty for congenital aortic stenosis: intermediate and late follow-up.
      The small size of the child at this stage often prohibits the use of an adult size prosthesis and therefore management strategies have evolved to include the use of either aortic leaflet repair or reconstruction until annular growth allows for a more durable prosthesis placement. Recent literature reports favorable comprehensive outcomes for the use of multiple techniques of aortic valve repair in children,
      • Vergnat M.
      • Asfour B.
      • Arenz C.
      • Suchowerskyj P.
      • Bierbach B.
      • Schindler E.
      • et al.
      Contemporary results of aortic valve repair for congenital disease: lessons for management and staged strategy.
      although the durability of many repair techniques is still debated.
      • Wilder T.J.
      • Caldarone C.A.
      • Van Arsdell G.S.
      • Pham-Hung E.
      • Gritti M.
      • Al Jughiman M.
      • et al.
      Aortic valve repair for insufficiency in older children offers unpredictable durability that may not be advantageous over a primary Ross operation.
      Ozaki and colleagues
      • Ozaki S.
      • Kawase I.
      • Yamashita H.
      • Uchida S.
      • Nozawa Y.
      • Takatoh M.
      • et al.
      A total of 404 cases of aortic valve reconstruction with glutaraldehyde-treated autologous pericardium.
      ,
      • Ozaki S.
      • Kawase I.
      • Yamashita H.
      • Uchida S.
      • Takatoh M.
      • Kiyohara N.
      Midterm outcomes after aortic valve neocuspidization with glutaraldehydetreated autologous pericardium.
      have reported extensively on the excellent outcomes for their technique of autologous pericardial aortic valve reconstruction. However, a study evaluating the outcomes in a younger population had a mean age of 47.8 ± 11.2 years.
      • Ozaki S.
      • Kawase I.
      • Yamashita H.
      • Nozawa Y.
      • Takatoh M.
      • Hagiwara S.
      • et al.
      Aortic valve reconstruction using autologous pericardium for patients aged less than 60 years.
      Therefore, the feasibility and outcomes of this aortic valve reconstruction technique has not been studied in children and young adults.
      We evaluated the immediate hemodynamic results and short-term outcomes for children and young patients who have undergone aortic leaflet replacement to determine the utility of this technique in the armamentarium of those managing aortic valve disease in pediatric populations.

      Methods

      Under institutional review board-approved protocols, we retrospectively reviewed the charts of 58 patients who underwent either neo-tricuspidalization (Ozaki procedure) or single leaflet reconstruction (SLR), with preservation and rotation of native leaflets, between 2015 and 2019. Immediate operative results as well as hospital and short-term outpatient follow-up data were evaluated.

      Data Collection

      Data were abstracted from inpatient hospital records, operative reports, follow-up, and clinic notes. Preadmission and immediate postrepair (intraoperative) echocardiograms were reviewed to assess immediate hemodynamic results of the repair. Follow-up echocardiograms were reviewed to assess durability over time. Severity of valvar stenosis was reported as peak velocity in meters per second (m/s). Aortic regurgitation (AR) was graded from 0 to 4 with grade 0 = none, grade 1 = trivial, grade 2 = mild, grade 3 = moderate, and grade 4 = severe.

      Operative Details

      Following median sternotomy, a large piece of autologous pericardium was harvested. This was then treated with 0.6% glutaraldehyde solution for 10 minutes, followed by rinsing in saline 3 × 6 minutes each.
      • Ozaki S.
      • Kawase I.
      • Yamashita H.
      • Uchida S.
      • Nozawa Y.
      • Matsuyama T.
      • et al.
      Aortic valve reconstruction using self-developed aortic valve plasty system in aortic valve disease.
      For patients aged 15 years or younger, the glutaraldehyde treatment was limited to 5 minutes. Tissue engineered bovine pericardium (CardioCel; Admedus, Queensland, Australia) was used in absence of native pericardium or due to regulatory restrictions on glutaradehyde use.
      After cardiac arrest with cold blood cardioplegia, a transverse aortotomy was performed. Retraction sutures were placed at each commissure for better exposure and to simulate the pressurized state of the aorta. The valvar anatomy was then inspected taking into account the number and position of commissures and raphes, leaflet geometry, and quality of the leaflet tissue. Based on this assessment a decision was made as whether to perform an Ozaki procedure or SLR with preservation of the native aortic valve tissue.
      In the case of neo-tricuspidalization, native leaflets were excised and leaflet replacement carried out in a manner as described by Ozaki and colleagues (Video 1).
      • Ozaki S.
      • Kawase I.
      • Yamashita H.
      • Uchida S.
      • Nozawa Y.
      • Matsuyama T.
      • et al.
      Aortic valve reconstruction using self-developed aortic valve plasty system in aortic valve disease.
      Multiple 5–0 polypropylene sutures were used to implant newly created cusps in patients weighing <20 kg.
      Figure thumbnail fx2
      Video 1The initial echocardiogram clips shows a bicuspid aortic valve with poor coaptation and severe aortic regurgitation in a 6-year old female patient. The native aortic valve leaflets are resected and sizers used to measure intercommissural distance and to mark a midpoint on the native annulus for position of new commissures. A template of corresponding size is then used to create each neo-cusp with marking of dots for suturing. Starting at the midpoint of the right coronary sinus, the neo-cusp is secured to the annulus with a running polypropylene suture with a 3:1 suturing ratio between cusp and annulus initially. After suturing the last marker dot, the suture is then passed through the aortic wall 2 mm below the level of the commissure. The left coronary neo-cusp is then placed in a similar fashion and both commissural sutures and wing extension passed through a felt pledget outside the aortic wall and tied thus creating the right/left commissure. The noncoronary neo-cusp is then placed in identical fashion with creation of the left/noncoronary and then non/right coronary commissure last. Immediate postoperative echocardiography reveals well opening neo-cusps with trivial central regurgitation. Video available at: https://www.jtcvs.org/article/S0022-5223(19)32356-6/fulltext.
      The SLR technique was carried out in a way similar to the description by Prêtre and colleagues.
      • Prêtre R.
      • Kadner A.
      • Dave H.
      • Bettex D.
      • Genoni M.
      Tricuspidisation of the aortic valve with creation of a crown-like annulus is able to restore a normal valve function in bicuspid aortic valves.
      Both of the fused leaflets were detached from a commissure/raphe along the annular level to an extent at which the leaflets could be rotated and brought high enough to form new commissures. Particular attention was paid for these to be of equal height compared with the reference commissure. The new leaflet was then measured and fashioned similar to the description by Hammer and colleagues.
      • Hammer P.E.1
      • del Nido P.J.
      Guidelines for sizing pericardium for aortic valve leaflet grafts.
      Lengths of silk suture were then used to estimate the required free edge length and geometric height of the new leaflet. These were then used as a guide to fashion a neo-cusp from either autologous glutaraldehyde-treated pericardium or bovine pericardium. The newly fashioned leaflet was then sewn to the annulus and aortic wall with either running 5–0 or 4–0 polypropylene suture, starting at the nadir of the new sinus with the neo-cusp folded into the outflow tract, and then carrying the suture line up to its respective commissures. It was secured to each commissure by passing a pledgeted polypropylene suture through the leaflet and out of the aortic wall. The height of the neo-cusp was then trimmed to an appropriate length and valve geometry as well as coaptation was reassessed.

      Statistical Analysis

      Categorical data are presented as percentage and continuous nonnormally distributed data are presented as median and interquartile range (IQR) or mean. Differences within a group, for normally distributed continuous variables, were compared by 2-tailed Student t tests and nonnormally distributed variables were compared by Wilcoxon test. Freedom from reoperation and moderate or greater AR was estimated by Kaplan-Meier analysis. Differences between groups were analyzed by log-rank test.
      Analyses were performed using R version 2018 (R Foundation for Statistical Computing, Vienna, Austria) and IBM SPSS software version 21.0 (IBM-SPSS Inc, Armonk, NY).

      Demographic Characteristics

      A total of 58 patients underwent aortic leaflet reconstruction surgery between 2015 and early 2019. The median age and weight of patients at the time of operation was 14.8 years (IQR, 10.6-16.8 years) and 53.5 kg (IQR, 32.9-67.8 kg). There were 23 balloon valvuloplasties performed in 22 patients before indexed surgery and 11 previous cardiac operations. The majority of patients (60%) had either isolated aortic stenosis in 14 (24%) or mixed pathology in 21 (36%) at the time of valve repair. The remaining 23 patients (40%) had AR. Details of the preoperative aortic valve anatomy and patient characteristics can be found in Table 1.
      Table 1Demographic characteristics of patient cohort (N = 58)
      CharacteristicResult
      Age at operation (y)14.8 (10.6-16.8)
      Weight (kg)53.5 (32.9-67.8)
      Preoperative aortic valve peak velocity (m/s)3.4 (2.3-4.2)
      Preoperative aortic regurgitation3 (3-4)
      Preoperative aortic valve annular diameter
      n = 55.
      (mm)
      21 (18-23.5)
      Preoperative aortic annular Z score1.11 (–0.1 to 3.2)
      Previous intervention23 (40)
      Aortic valve anatomy
       Monocuspid8
       Bicuspid34
       Tricuspid15
       Quadricuspid1
      Previous operations11 (19)
       Aortic valve repair2
       Heart transplant1
       CAT repair with repair of truncal valve1
       Subaortic membrane resection1
       DORV repair1
       Coarctation repair1
       Surgical aortic valvotomy1
       Supravalvar AS repair1
       PAB/coarctation repair1
       Aortic valve repair after previous ASO for TGA1
      Values are presented as median (interquartile range) or (%). CAT, Common arterial trunk; DORV, double-outlet right ventricle; AS, aortic stenosis; PAB, pulmonary artery band; ASO, arterial switch operation; TGA, transposition of the great arteries.
      n = 55.

      Results

      Operative Characteristics

      Of 58 patients, 40 patients (69%) underwent an Ozaki procedure. The remaining 18 patients (31%) underwent SLR. The material used for leaflet reconstruction was split, with 26 patients (45%) receiving autologous pericardium and 32 patients (55%) bovine pericardium (CardioCel). Twelve patients (21%) had concomitant procedures performed at the time of aortic valve surgery (Table 2). The median bypass and crossclamp times of those patients undergoing isolated Ozaki or SLR were 130.5 minutes (IQR, 113.5-142.5 minutes) and 103.5 minutes (IQR, 90.5-111 minutes), respectively. Forty patients (69%) were extubated on the day of surgery. The median intensive care unit and hospital length of stay was 1 day (IQR, 1-2 days) and 5 days (IQR, 4-7 days), respectively. Further perioperative characteristics can be found in Table 2.
      Table 2Operative characteristics (N = 58)
      CharacteristicResult
      Technique
       Ozaki40 (69)
       Single leaflet reconstruction18 (31)
      Patients with concomitant procedures12 (21)
       RV-PA conduit1
       Mitral valve repair1
       Supravalvar AS repair1
       Reduction aortoplasty3
       Resection of subaortic membrane2
       PDA ligation1
       PA debanding/septal myectomy/ASD creation1
       Septal myectomy1
       Manougian root enlargment/supravalvar AS repair1
      Cusp material
       Autologous pericardium26 (45)
       Bovine pericardium32 (55)
      Bypass time (min)130.5 (113.5-142.5)
      Crossclamp time (min)103.5 (90.5-111)
      Postoperative aortic valve peak velocity (m/s)2 (1.75-2.4)
      Postoperative aortic regurgitation degree1 (0-1)
      ICU length of stay (d)1 (1-2)
      Hospital length of stay (d)5 (4-7)
      Values are presented as n (%) or median (interquartile range). RV-PA, Right ventricular to pulmonary artery; AS, aortic stenosis; PDA, patent ductus arteriosus; PA, pulmonary artery; ASD, atrial septal defect; ICU, intensive care unit.

      Echocardiographic Follow-up

      Follow-up was complete in all but 1 patient. Statistical comparison shows that both Ozaki procedure and SLR were able to achieve significant reduction in aortic valve peak velocity from 3.4 ± 1.2 m/s to 2.0 ± 0.4 m/s immediately following repair (t test P < .001) and this did not significantly increase (2.2 ± 0.7 m/s) over a median echocardiographic follow up of 14.1 months (IQR, 7.2-20.1 months) (Figure 1).
      Figure thumbnail gr1
      Figure 1Box plots depicting aortic valve peak velocities preoperatively, immediately postoperatively, and at follow-up for the entire cohort.
      When evaluated separately, both Ozaki procedure and SLR groups were able to achieve a significant reduction in aortic valve peak velocity following repair: Ozaki group from 3.1 ± 1.1 m/s to 1.9 ± 0.4 m/s (t test P < .001) and SLR group from 4.1 ± 1.2 m/s preoperatively to 0.8 ± 0.4 m/s postoperatively (t test P < .001). Although aortic valve peak velocities immediately following repair and at follow-up in patients where autologous pericardium was used were not different (1.91 ± 0.38 vs 1.83 ± 0.77; t test P = .68) there was a significant increase in velocity of patients repaired with bovine pericardium over time (2.13 ± 0.42 vs 2.58 ± 0.56; t test P = .002) (Figure 2).
      Figure thumbnail gr2
      Figure 2Box plots depicting the median and interquartile ranges of aortic valve peak velocities in meters per second preoperatively (blue), immediately postoperatively (red), and at follow-up (green) stratified by leaflet material used for repair. AS, Aortic stenosis.
      Correlations of annular size and aortic valve peak velocity after Ozaki procedure at follow-up were examined using correlation analysis for both types of patch material. The correlation coefficients were compared with a 2-sided Fisher independent z test (P = .2338) and Zou confidence interval (95% CI), –0.9257 to 0.2087. No significant difference was observed. (Figure 3).
      Figure thumbnail gr3
      Figure 3Correlations of annular size (millimeters) and aortic valve peak velocity (meters per second) after Ozaki procedure at follow-up was examined using correlation analysis for both types of leaflet material.
      Of 44 patients with moderate or greater AR before repair, all were reduced to mild or less immediately after surgery (44 vs 0; Wilcoxon P < .001). All but 2 patients, both from the SLR group, had mild or less AR at the final follow-up.
      There was 1 early reoperation after neo-tricuspidalization with partial right neo-cusp detachment that was addressed on the first postoperative day without need for further interventions. This represents a technical failure; hence, it was considered separately from late reoperations, which were due to either endocarditis or structural valve degeneration.
      Six patients (10%) required late reoperation (Ozaki group n = 4 and SLR group n = 2). A summary of indications and time to reintervention for the entire cohort is presented in Table 3.
      Table 3Summary of indications and time to reintervention for the entire cohort
      Patients requiring reoperationIndex surgeryMaterialIndication for reinterventionTime to re-intervention (mo)Reintervention
      1
      Successful preservation of the initial leaflet reconstruction surgery.
      SLRBovine pericardiumNeo-cusp perforation2.8Patch repair
      2
      Successful preservation of the initial leaflet reconstruction surgery.
      OzakiBovine pericardiumEndocarditis9.1Valve repair
      3OzakiBovine pericardiumEndocarditis/root abscess11.0Homograft root replacement
      4OzakiAutologous pericardiumEndocarditis19.6Mechanical prosthesis implantation
      5SLRAutologous pericardiumSVD20.4Ross procedure
      6OzakiBovine pericardiumSVD27.8Mechanical prosthesis implantation
      Values are presented as time from initial cusp replacement surgery to reintervention in months. SLR, Single leaflet reconstruction; SVD, structural valve degeneration (reduced neo-cusp mobility).
      Successful preservation of the initial leaflet reconstruction surgery.
      For the Ozaki procedure, reoperations were due to endocarditis in 3 patients and structural valve degeneration (decreased mobility and calcification of bovine pericardial leaflet) in 1 patient. One patient had successful preservation of the initial neo-tricuspidalization after developing group A Streptococcus endocarditis associated with varicella zoster virus infection. This patient had reoperation following 6 weeks of antibiotic treatment with closure of periannular abscess cavities. Of the other 2 patients with endocarditis, 1 received a mechanical valve implantation and one had a homograft root replacement for associated aortic root destruction. The patient with degenerated bovine pericardial leaflets and reduced neo-cusp mobility had mechanical valve replacement. Of the 2 reoperations in the SLR group, 1 patient underwent a Ross procedure and another with the neo-cusp perforation was able to undergo repair with a patch closure.
      The durability of the repair was investigated as freedom from either late reoperation or moderate and greater AR at 1, 2, and 3 years and was 94.2% ± 3.3%, 85.0% ± 5.8%, and 79.0% ± 8.0%, respectively, without a difference when evaluated according to surgical technique (P = .635) or leaflet material used (P = .464) (Figures 4 and 5). When patients who underwent neo-tricuspidalization with autologous pericardium were evaluated separately, the freedom from reoperation and moderate or greater AR was 87.5% at the time of final follow-up (Figure 6).
      Figure thumbnail gr4
      Figure 4This Kaplan-Meier curve depicts freedom from reoperation and ≥ moderate aortic regurgitation (AR) at follow-up, stratified by index operation (Ozaki vs single leaflet reconstruction [SLR]). 95% CI, 95% Confidence interval.
      Figure thumbnail gr5
      Figure 5Kaplan-Meier curve depicting freedom from reoperation and moderate or severe aortic regurgitation (AR) following complex aortic valve repair stratifed by leaflet material (autologous pericardium vs bovine pericardium). 95% CI, 95% Confidence interval.
      Figure thumbnail gr6
      Figure 6Kaplan-Meier curve depicting freedom from reoperation and moderate to severe aortic regurgitation (AR) in patients undergoing Ozaki procedure where autologous pericardium was used for leaflet reconstruction. 95% CI, 95% Confidence interval.
      There was 1 mortality in a patient with a history of prior heart transplant for dilated cardiomyopathy and severely impaired left ventricle function, 5.6 months after discharge following aortic valve reconstruction surgery. The transplant was complicated by infective endocarditis of the donor heart requiring resection of a vegetation and resultant AR. This patient also experienced heart block requiring permanent pacemaker placement after heart transplant. At the time of aortic valve surgery, his left ventricular shortening fraction was 13% with left ventricular end diastolic diameter of 56.5 mm and left ventricular end systolic diameter of 48.9 mm. He underwent neo-tricuspidalization and was discharged after 28 days. A 5-month follow-up echocardiogram demonstrated only mild AR and peak transvalvar velocity of 2.8 m/s. His clinical condition was improved with left ventricle shortening fraction of 19%, left ventricular end diastolic diameter of 42.4 mm and left ventricular end systolic diameter 34.5 mm. His death occurred outside the hospital and therefore the exact details remain uncertain.

      Discussion

      The management of aortic valve disease in the pediatric population presents a significant challenge with the overall goals of preserving the left ventricle function and minimizing the number of procedures required over a lifetime. However, multiple factors influence which interventional strategies can be applied, most importantly the patient's underlying cardiac anatomy and the age at which they reach indications for aortic valve intervention. Aortic leaflet replacement techniques can provide a useful alternative for patients with particular anatomic challenges.
      The initial management strategy for aortic stenosis in the neonatal population has historically been the use of balloon valvuloplasty; however, several publications have advocated for the superior freedom from reoperation provided by surgical valve repair.
      • Donald J.S.
      • Konstantinov I.E.
      Surgical aortic valvuloplasty versus balloon aortic valve dilatation in children.
      ,
      • Hill G.D.
      • Ginde S.
      • Rios R.
      • Frommelt P.C.
      • Hill K.D.
      Surgical valvotomy versus balloon valvuloplasty for congenital aortic valve stenosis: a systematic review and meta-analysis.
      More recent re-evaluations of balloon valvuloplasty have revealed very poor outcomes when urgent/emergent aortic valve replacement is required following this technique.
      • Woods R.K.
      • Pasquali S.K.
      • Jacobs M.L.
      • Austin E.H.
      • Jacobs J.P.
      • Krolikowski M.
      • et al.
      Aortic valve replacement in neonates and infants: an analysis of the Society of Thoracic Surgeons Congenital Heart Surgery Database.
      Many centers, including our own, have transitioned to a policy of surgical valvotomy for the initial management of aortic stenosis apart from neonates presenting with either severe left ventricular impairment and/or poor clinical condition in which case a balloon valvotomy is still considered a valuable alternative.
      The choice of the next operation is another area of even more significant debate. The Ross procedure clearly provides several advantages.
      • Al-Halees Z.
      • Pieters F.
      • Qadoura F.
      • Shahid M.
      • Al-Amri M.
      • Al-Fadley F.
      The Ross procedure is the procedure of choice for congenital aortic valve disease.
      However, an increasing number of reports have shown significant incidence of autograft dilation within the first 2 decades following Ross procedure.
      • Elkins R.C.
      • Thompson D.M.
      • Lane M.M.
      • Elkins C.C.
      • Peyton M.D.
      Ross operation: 16-year experience.
      ,
      • David T.E.
      • Omran A.
      • Ivanov J.
      • Armstrong S.
      • de Sa M.P.
      • Sonnenberg B.
      • et al.
      Dilation of the pulmonary autograft after the Ross procedure.
      This late complication can be addressed by performing a valve-sparing aortic root procedure in some patients.
      • de Kerchove L.
      • Boodhwani M.
      • Etienne P.Y.
      • Poncelet A.
      • Glineur D.
      • Noirhomme P.
      • et al.
      Preservation of the pulmonary autograft after failure of the Ross procedure.
      Further studies have suggested use of an inclusion technique as a primary procedure, that while protecting the autograft from dilation, also fixes the aortic root diameter and can only be applied in patients with an adequately sized pulmonary valve.
      • de Kerchove L.
      • Rubay J.
      • Pasquet A.
      • Poncelet A.
      • Ovaert C.
      • Pirotte M.
      • et al.
      Ross operation in the adult: long-term outcomes after root replacement and inclusion techniques.
      Our center has recently published data reporting on the subannular technique for autograft placement that demonstrates protection of the autograft from dilation and also allows for continued somatic growth of the aortic annulus; however, it is unclear if this benefit extends beyond the first decade after surgery.
      • Tran P.K.
      • Tsang V.T.
      • Cornejo P.R.
      • Torii R.
      • Dominguez T.
      • Tran-Lundmark K.
      • et al.
      Midterm results of the Ross procedure in children: an appraisal of the subannular implantation with interrupted sutures technique.
      The Ross operation was also shown to have suboptimal results when used in a population with bicuspid aortic valves and AR.
      • Favaloro R.
      • Stutzbach P.
      • Gomez C.
      • Machain A.
      • Casabe H.
      Feasibility of the ross procedure: its relationship with the bicuspid aortic valve.
      The advantages of the Ross procedure are also conflicted by the potential future need for reintervention on the right ventricular to pulmonary artery conduit with a reported freedom from homograft reintervention of 87.5% at 20 years.
      • Oeser C.
      • Uyanik-Uenal K.
      • Kocher A.
      • Laufer G.
      • Andreas M.
      Long-term performance of pulmonary homografts after the Ross procedure: experience up to 25 years.
      Another option is placement of a mechanical prosthesis with or without annular enlargement. This provides acceptable freedom from reoperation, most recently found to be 78.4% ± 6.9% at 10 years in a cohort with a median age of 16 years (IQR, 12-22.8 years) with younger age acting as a significant independent predictor for reoperation. The rate of thromboembolism was found to be 0.66% per patient-year and bleeding 0.83% per patient year in a cohort managed on warfarin anticoagulation with goal international normalized ratio of 2.0 to 3.0. In this study 33% of patients were also treated with aspirin and 1 with clopidogrel.
      • Myers P.O.
      • Mokashi S.A.
      • Horgan E.
      • Borisuk M.
      • Mayer Jr., J.E.
      • Del Nido P.J.
      • et al.
      Outcomes after mechanical aortic valve replacement in children and young adults with congenital heart disease.
      A recently published meta-analysis with microsimulation by Korteland and colleagues
      • Korteland N.M.
      • Etnel J.R.G.
      • Arabkhani B.
      • Mokhles M.M.
      • Mohamad A.
      • Roos-Hesselink J.W.
      • et al.
      Mechanical aortic valve replacement in non-elderly adults: meta-analysis and microsimulation.
      has shown a substantial late mortality of 1.55% per patient year in nonelderly patients undergoing mechanical aortic valve replacement, with mean life expectancy just more than half of the age-matched general population. This difference has been even more significant in younger population.
      There are patients in whom mechanical aortic valve replacement or the Ross procedure is not applicable. For example, patients with previous truncus arteriosus repair and others lacking a suitable pulmonary autograft, will not have a viable option for the Ross procedure. Also, many pediatric patients will not have an adequate aortic annular size to accommodate a prosthesis that will be large enough to avoid reoperation following significant patient growth. Furthermore, implantation of a small stented valve fixes the annulus, making reimplantation surgery challenging due to the necessity of performing an annular enlargement. These patients, in whom a definitive adult size aortic valve replacement procedure cannot be performed, have the most to benefit from leaflet replacement techniques.
      Our investigation has shown that both an Ozaki procedure and SLR can be performed in pediatric populations, with annular size as small as 6.7 mm (SLR), with excellent immediate hemodynamic outcomes. We believe that the advantages of the Ozaki procedure with increased free margin length of the neo-cusps as discussed by Ozaki and colleagues
      • Ozaki S.
      • Kawase I.
      • Yamashita H.
      • Uchida S.
      • Nozawa Y.
      • Takatoh M.
      • et al.
      Reconstruction of bicuspid aortic valve with autologous pericardium—usefulness of tricuspidization.
      will have an even greater utility in pediatric populations. We anticipate that with annular and sinotubular junction growth, the coaptation may potentially be preserved by the excess of effective coaptation height at the time of initial repair.
      • Ozaki S.
      • Kawase I.
      • Yamashita H.
      • Uchida S.
      • Nozawa Y.
      • Takatoh M.
      • et al.
      Reconstruction of bicuspid aortic valve with autologous pericardium—usefulness of tricuspidization.
      This has been shown to be a strong predictor of aortic valve repair durability.
      • Bierbach B.O.
      • Aicher D.
      • Issa O.A.
      • Bomberg H.
      • Gräber S.
      • Glombitza P.
      • et al.
      Aortic root and cusp configuration determine aortic valve function.
      An additional advantage of this technique is anticipated preservation of annular dynamic parameters and unhindered growth of the aortic annulus, which allows for further aortic leaflet reconstruction surgery. Also, continued aortic annular growth allows for the avoidance of aortic root enlargement techniques when aortic valve replacement becomes necessary in the future.
      A recognized area of concern in our study is the 5% incidence of infective endocarditis. Etnel and colleagues
      • Etnel J.R.
      • Elmont L.C.
      • Ertekin E.
      • Mokhles M.M.
      • Heuvelman H.J.
      • Roos-Hesselink J.W.
      • et al.
      Outcome after aortic valve replacement in children: a systematic review and meta-analysis.
      recently published a meta-analysis of the outcomes after aortic valve replacement in children reporting a rate of endocarditis of 0.40% per year (IQR, 0.22%-0.73% per year) following Ross, 0.45% per year (IQR, 0.27%-0.75% per year) following mechanical prosthesis, and 0.66% per year (IQR, 0.25%-1.75% per year) following homograft aortic valve replacement.
      • Etnel J.R.
      • Elmont L.C.
      • Ertekin E.
      • Mokhles M.M.
      • Heuvelman H.J.
      • Roos-Hesselink J.W.
      • et al.
      Outcome after aortic valve replacement in children: a systematic review and meta-analysis.
      Ozaki and colleagues
      • Ozaki S.
      • Kawase I.
      • Yamashita H.
      • Uchida S.
      • Takatoh M.
      • Kiyohara N.
      Midterm outcomes after aortic valve neocuspidization with glutaraldehydetreated autologous pericardium.
      reported 13 cases of infective endocarditis requiring aortic valve reoperation among 850 cases (1.5%) after a mean follow-up of 53.7 ± 28.2 months. This brings into question the propensity of the leaflet material for bacterial inoculation. A study investigating the high incidence of right heart endocarditis in patients with congenital heart disease after surgery or percutaneous pulmonary valve implantation compared 3 different materials for valved stents. Bovine pericardium was found to have the lowest propensity of bacterial adhesion in comparison to bovine jugular vein and porcine pericardium.
      • Jalal Z.
      • Galmiche L.
      • Lebeaux D.
      • Villemain O.
      • Brugada G.
      • Patel M.
      • et al.
      Selective propensity of bovine jugular vein material to bacterial adhesions: an in-vitro study.
      It is unclear which factors contributed to incidence of endocarditis in our cohort. One patient developed a vegetation following infection with varicella zoster virus, which is a described complication.
      • Kostolny M.
      • Malik T.
      • Bonello B.
      Infective endocarditis associated with varicella zoster virus following aortic valve repair.
      Another patient developed endocarditis as a consequence of poor dental hygiene. Additional follow-up and comparison of incidence of endocarditis following alternative valve operations at our institution will be required to discern this definitively.
      The variability in patient pathologic substrates and aortic valve repair techniques performed makes a meaningful comparison of our results with the literature difficult to carry out. One center has published freedom from reintervention at 1, 5, and 7 years of 97%, 87%, and 80%, respectively, for patients undergoing valve repair. Multiple techniques were used in these patients, which included leaflet extension, tricuspidization, commissurotomy, leaflet thinning, triangular resection, subcommissural annuloplasty, free-edge plication, and leaflet perforation repair.
      • d'Udekem Y.
      • Siddiqui J.
      • Seaman C.S.
      • Konstantinov I.E.
      • Galati J.C.
      • Cheung M.M.
      • et al.
      Long-term results of a strategy of aortic valve repair in the pediatric population.
      Also, a more recent article described results of aortic valve repair in a population with a median age of 9.79 years (IQR, 0.1-28.7 years). Techniques used in this population included commissurotomy shaving (38%), leaflet replacement (40%), leaflet extension (11%), and neocommissure creation (11%) with a freedom from reoperation at 1, 5, and 7 years of 89%, 70%, and 57%, respectively.
      • Vergnat M.
      • Asfour B.
      • Arenz C.
      • Suchowerskyj P.
      • Bierbach B.
      • Schindler E.
      • et al.
      Contemporary results of aortic valve repair for congenital disease: lessons for management and staged strategy.
      The most common reason for reoperation in this study was substantial AR. These outcomes must be considered with caution given the fundamental differences in the repair techniques used in these studies and our patient cohort.
      Identification of an optimal leaflet replacement material is a particularly difficult endeavor. This is likely to be the “Achilles' heel” of leaflet replacement surgeries in young patients rather than surgical technique per se. Scarce clinical evidence exists in determining which biomaterial for aortic leaflet replacement would be optimal.
      • Toeg H.D.
      • Abessi O.
      • Al-Atassi T.
      • de Kerchove L.
      • El-Khoury G.
      • Labrosse M.
      • et al.
      Finding the ideal biomaterial for aortic valve repair with ex vivo porcine left heart simulator and finite element modeling.
      An increased risk of long-term recurrent AR following aortic valve repair has been associated with the use of a patch in a number of studies that used a variety of materials.
      • Boodhwani M.
      • de Kerchove L.
      • Glineur D.
      • Rubay J.
      • Vanoverschelde J.L.
      • Noirhomme P.
      • et al.
      Repair of regurgitant bicuspid aortic valves: a systematic approach.
      ,
      • Lausberg H.F.
      • Aicher D.
      • Langer F.
      • Schäfers H.J.
      Aortic valve repair with autologous pericardial patch.
      Glutaraldehyde fixed autologous pericardium has provided acceptable durability in elderly patients following the Ozaki procedure; however, the results from this study cannot be directly extrapolated to pediatric populations. It has been shown that biomaterials are prone to more rapid degeneration in younger patients, especially children.
      • Rodriguez-Gabella T.
      • Voisine P.
      • Puri R.
      • Pibarot P.
      • Rodés-Cabau J.
      Aortic bioprosthetic valve durability: incidence, mechanisms, predictors, and management of surgical and transcatheter valve degeneration.
      In a recently published study by Nordmeyer and colleagues,
      • Nordmeyer S.
      • Murin P.
      • Schulz A.
      • Danne F.
      • Nordmeyer J.
      • Kretzschmar J.
      • et al.
      Results of aortic valve repair using decellularized bovine pericardium in congenital surgery.
      the use of CardioCel in patients with congenital aortic valve disease (median age, 9 years) was associated with unsatisfactory mid-term results. In our series, the explanted bovine patch material showed evidence of calcification on histopathology (Figure 7). However, it was unclear whether this process started within the patch or it extended from either the aortic annulus or suture line.
      Figure thumbnail gr7
      Figure 7Histopathology of explanted right coronary CardioCel patch (Admedus, Queensland, Australia) stained with Alcian blue/periodic acid Schiff.
      We have demonstrated better performance of autologous pericardium compared to bovine pericardium with lower gradient across the aortic valve at final follow-up. However, we did not observe a significant difference in terms of material used for a composite outcome measure of AR, endocarditis, or reoperation rate. However, a 100% freedom from moderate to severe AR at follow-up in the Ozaki group where autologous pericardium was used (n = 20) could be an indicator of favorable midterm results.

      Limitations

      Our study has limitations inherent to any retrospective review. Particularly, our study does not allow for the direct comparison of this cohort with patients receiving alternative procedures at our institution and relies on the extrapolation of previously published outcome data. Future directions of investigation will need to validate midterm durability, the influence of different materials used for cusp reconstruction, and the timing of progression to definitive aortic valve operations.

      Conclusions

      Complex aortic valve repair using aortic leaflet replacement techniques can be applied in children and young adults with acceptable immediate hemodynamic outcomes. The guarded need for reintervention of this technique must be weighed against the need for late autograft reintervention, pulmonary homograft replacement, and the anticoagulation-related morbidity of aortic valve replacement. In addition, aortic leaflet replacement techniques may offer utility in pediatric patients with anatomy unsuitable for aortic valve replacement.

      Conflict of Interest Statement

      Mr Martin Kostolny has proctorship contract with TERUMO EUROPE NV, Belgium. All other authors have nothing to disclose with regard to commercial support.

      Supplementary Data

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      Linked Article

      • Commentary: Aortic valve reconstruction and the Ozaki procedure in children—Finding the best fit
        The Journal of Thoracic and Cardiovascular SurgeryVol. 159Issue 6
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          Aortic valve disease continues to be a challenging problem in pediatric patients. We continuously search for new innovations, as our best options are imperfect. In this issue of the Journal, Wiggins and colleagues1 from Great Ormond Street present their short-term results using the Ozaki procedure (neotricuspidization) and other valve reconstruction techniques in children and young adults. This is currently the largest retrospective single-center review in children and young adults, comprising 58 patients from 2015 to 2019.
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        • PDF
        Open Archive
      • Commentary: Are pediatric aortic leaflet reconstructions a long run for a short slide or a home run?
        The Journal of Thoracic and Cardiovascular SurgeryVol. 159Issue 6
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          In this issue of the Journal, Wiggins and colleagues1 present their work studying the utility of aortic valve leaflet reconstruction in children and young adults with aortic valve disease. Using data from a high-volume, single center, the authors studied 58 patients over a 4-year period who underwent either an aortic valve neo-tricuspidization procedure (Ozaki) or a single-leaflet reconstruction. The authors found that these 2 techniques can be performed safely with acceptable short-term hemodynamics in a population of patients that remains a significant clinical challenge.
        • Full-Text
        • PDF
        Open Archive
      • Commentary: Continue to imitate the nature: We are getting closer
        The Journal of Thoracic and Cardiovascular SurgeryVol. 159Issue 6
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          A sustained long-term treatment strategy for the treatment of aortic valve disease in the pediatric population is inevitable. Thus, this strategy should involve the entire current armamentarium of available treatment options that need to be applied individually in each and every case. The requirements for the ideal valve substitute are well known, whereas such a valve is still not available.1 A myriad of factors influence the decision-making in this population that starts with the anatomy of the valve, concomitant cardiac lesions, previous interventions, patient needs and choice, and particularly the expertise of the surgical team.
        • Full-Text
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        Open Archive