Eur J Cardiothorac Surg 2008;33:548-553. doi:10.1016/j.ejcts.2007.12.044
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
Truly stentless molded autologous pericardial aortic valve prosthesis with single point attached commissures in a sheep model
Wolfgang A. Goetzb,*,
Teing Ee Tanc,
Khee Hiang Limd,
Sidney Le Hung Salguesa,
Nil Groussona,
Fangli Xionga,
Yeow Leng Chuac,
Joon Hock Yeoa
a Nanyang Technological University, School of Mechanical and Aerospace Engineering, Division of Thermal and Fluids Engineering, Singapore, Singapore
b Department of Cardiovascular Surgery, German Heart Center at the Technical University Munich, Munich, Germany
c National Heart Centre at Singapore General Hospital, Singapore, Singapore
d Auckland University of Technology, Auckland, New Zealand
Received 17 October 2007;
received in revised form 23 December 2007;
accepted 29 December 2007.
* Corresponding author. Address: German Heart Center Munich, Lazarettstr. 36, 80636 Munich, Germany. Tel.: +49 89 1218 0; fax: +49 89 1218 4113. (Email: goetz{at}dhm.mhn.de).
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Abstract
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Objective: Aortic valve cusp extension and free-hand aortic valve replacement with autologous pericardium has been described. The long-term results were shown to be comparable with commercially available aortic bioprostheses. Nevertheless the relatively demanding surgical technique could not find wide acceptance. We developed a new design of a molded aortic valve, fashioned from autologous pericardium, treated briefly with glutaraldehyde, and simplified the implantation technique using single point attached commissures (SPAC). Methods: Molded autologous valve prostheses were implanted in the subcoronary aortic position in 10 sheep with the commissures connected to the aortic wall at three single commissural points (SPAC). The prosthesis mean size was 21.6 ± 1.3 mm and the construction time (excluding 10 min glutaraldehyde treatment) was 6.2 ± 1.2 min. Cardiopulmonary bypass and cross-clamp time was 111.1 ± 12.4 min and 75.0 ± 16.3 min, respectively. Six sheep were euthanized after 201.2 ± 10.3 days (6 months) and four sheep were euthanized after 330.8 ± 6.5 days (11 months) postoperatively. Results: In all sheep, the valve was immediately competent. At sacrifice, SPAC has proven to be well anchored to the aortic wall and the pericardial valve to be pliable in all cases. The maximum transvalvular gradient after cardiopulmonary bypass and at sacrifice was 3.7 ± 2.2 mmHg and 10.6 ± 5.2 mmHg, respectively. Conclusions: This new truly stentless molded autologous aortic valve with simplified implantation technique (SPAC) makes a reliable implantation in a standard timeframe possible. The simplicity of construction, low cost and absent need for anticoagulation of this molded autologous aortic bioprosthesis offers an attractive alternative and not only for patients in the developing world.
Key Words: Autologous pericardium • Aortic valve prosthesis • Stentless
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1. Introduction
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The molded autologous pericardial aortic valve prosthesis, treated briefly with glutaraldehyde was introduced in 1988 by Carlos Duran [1] but hampered by the complex implantation technique. The running suture that follows the scalloped shape of the stentless valve is difficult to perform and prone to either distort the geometry of the valve or compromise the coronary flow due to vagaries in the position of the coronary ostia. In order to simplify implantation technique we hypothesized that the autologous aortic valve should be implanted with a technique similar to the proximal suture used for the implantation of stentless auto-, homo- or xenografts. Additionally we intended to construct a stentless valve reducing suture material to a minimum that should allow maximum flexibility of the leaflets and because sutures are known to be a nidus for tissue calcification [2].
These premises prompted us to design the ‘temporarily stented autologous aortic valve’ with flat leaflets using the single point attached commissure (SPAC) implantation technique [3,4].
Molding of the pericardial leaflets in a three-dimensional geometry closer to the natural valve was found to positively influence leaflet stress distribution and coaptation and especially reduces stress at the commissures [5]. Consequently molding of pericardial aortic valve prosthesis was combined with SPAC implantation technique. A new valve mold was designed that allows to shape and trim the pericardium in order to construct a truly stentless aortic valve with SPACs.
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2. Material and methods
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Ten adult sheep (bodyweight 53 ± 7.1 kg) underwent aortic valve replacement with a molded autologous pericardium prosthesis treated for 10 min with glutaraldehyde.
All animals received humane care in accordance with the Principles of Laboratory Animal Care formulated by the Animal Welfare Act in the Guide for Care and Use of Laboratory Animals prepared by the Institute of Laboratory Animal Resources and published by the National Institutes of Health, Singapore (NIH publication No. 85–23, revised 1996).
The animals were premedicated with ketamine 1.0 mg/kg, atropine 0.03 mg/kg, and propofol 4.0 mg/kg body weight. The ECG was monitored continuously with four leads. Arterial pressure was monitored through a pressure catheter in the axilla artery. Animals were intubated and ventilation was achieved with a volume-regulated respirator (North American Drager, Telford, Pennsylvania, USA) and oxygen at a flow of 4 l/min. Anesthesia was maintained with isoflurane at a gas level of 0.5–1.0% as needed. The animal was then placed in the right lateral decubitus position. The heart was exposed with a standard left thoracotomy through the 4th intercostal space.
The mediastinal surface of the pericardium was dissected free of fat and connective tissue. A rectangular piece of pericardium extending from the left phrenic nerve to the midline was resected and placed on a wet towel where further cleaning of its mediastinal surface was done.
Epicardial echocardiography was performed to measure aortic annulus and sinotubular junction diameter in order to determine the appropriate mold size.
Heparin 300 U/kg i.v. was injected as a bolus in preparation for cardiopulmonary bypass with a target ACT of 
480 s. A 16 Fr arterial cannula was inserted into the descending aorta and 32 Fr double stage venous cannula into the right atrial appendage. Once cardiopulmonary bypass was established a LV-vent line was inserted through the left atrium. The ascending aorta was cross-clamped proximal of the single brachiocephalicus trunk followed by the infusion of cold blood cardioplegia at 4 °C into the aortic root (Medtronic DLP Standard 9 Fr). Antegrade cold blood cardioplegia was repeated every twenty min by separate intubation of the left and right coronary ostium (CalMed California Medical Laboratories, CA, USA, Inc.; 10–14 Fr. coronary artery perfusion cannula or 4–6 mm coronary artery perfusion cannula w/balloon). A high transverse aortotomy was performed, approximately 1 cm distal of the sinotubular junction. The native aortic valve was excised and the aortic diameter at the sinotubular junction was measured. The diameters of the aortic annulus and the sinotubular junction measured with epicardial echocardiography immediately after pericardiotomy were concordant with the dimensions measured after transection of the aortic root using ball-sizers.
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3. Construction of autologous pericardial aortic valve prosthesis and surgical implantation
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Plastic molds for fashioning the pericardial valve prosthesis were available in sizes 15–29 mm diameter with 2 mm size increments. Once cleaned, the pericardium was sandwiched between the selected molds (Figs. 1 and 2
) and placed in a container with 0.5% buffered glutaraldehyde at room temperature for 10 min followed by rinsing in three separate bowls with ringer-lactate for at least 10 min. The pericardium was then trimmed down. The lateral sides were sutured together with a running 5-0 polypropylene suture that converted the molded pericardium into a three-leaflet valve (Fig. 3
).
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Fig. 3. The lateral sides of the pericardial strip were sutured together with only one running 5-0 polypropylene suture (sutured commissure in the back) that converted the molded pericardium into a truly stentless three-leaflet valve.
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The prosthesis was implanted with a proximal running 4-0 monofilament prolene sutures placed along the aortic annulus. Three single double-ended 4-0 ‘U’ sutures were passed at the commissures of the prosthesis. The locations of the new commissures in the ascending aorta were then determined by pulling the valve-commissures straight upward, ensuring to be equidistant. The sutures were passed through the aortic wall at the points determined by the height of the prosthesis. These sutures were tied over a pericardial pledget outside the aorta. From our previous experiments in vitro [4] and in sheep (unpublished) we learned that the suture at the single point attached commissures are prone to cut through the aortic wall when not supported by a pledget.
The aortotomy was closed with a running 4-0 suture after de-airing and the aorta was unclamped. The animal was weaned off bypass according to LV contractility; inotropic support was instituted for a short period. Once normal rhythm had returned, an epicardial 2D color echocardiographic study was performed to assess valve competence. Simultaneous pressure readings were taken using Millar pressure transducer control unit (TCB 600) and Mikro-Tip® Pressure Transducer Catheters SPC 330A (Millar Instruments, Inc., Houston, TX, USA) in the ascending aorta approximately 5–10 mm above commissural level and in the left ventricle to determine the transvalvular gradient. Intercostals nerve block with 0.25% bupivacaine was given for postoperative analgesia. The chest was closed in layers after insertion of a drain tube that was kept for a few hours. The animal was awoken immediately, extubated and transferred to the holding pen. All animals received antibiotic coverage with ceftiofur–sodium 3 mg/kg and gentamicin 80 mg i.m. for 3 days.
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4. Sacrifice
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At the time of sacrifice, under general anesthesia the thoracotomy was re-entered. An epicardial echocardiogram was recorded as well as simultaneous left ventricular and ascending aorta pressures. Under full heparinization the heart was excised, the left ventricle and ascending aorta opened and the macroscopic findings recorded and photographed.
The harvested specimens were preserved in 10% phosphate buffered formalin (Sigma–Aldrich, USA) for 2 days. Specimens were processed in a tissue processor (Leica TP1020, Germany) where they underwent dehydration through serial baths treatments, containing ascending concentration of ethanol, and finally being impregnated in a hot wax bath prior to blocking in wax. The tissue blocks were then sectioned into 7 µm thick slices using a rotary microtome (Leica RM2135, Germany) in longitudinal section through the middle of each cusp and a transverse section crossing each commissure. Representative sections were stained with hematoxylin/eosin for general tissue and cellular morphology and Masson's trichome for connective tissue.
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5. Results
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The mean size of the molded autologous pericardial aortic prosthesis was 21.6 ± 1.3 mm and the construction time (excluding 10 min glutaraldehyde treatment and 10 min rinsing) was 6.2 ± 1.2 min. Cardiopulmonary bypass and cross-clamp time was 111.1 ± 12.4 min and 75.0 ± 16.3 min, respectively. All 10 sheep survived until sacrifice. Six sheep were euthanized after 201.2 ± 10.3 days (6 months) and four sheep were euthanized after 330.8 ± 6.5 days (11 months) postoperatively. At sacrifice in all sheep the pericardial leaflets appeared pliable and were macroscopically free of pannus-growth or calcification (Fig. 4
). Specific observations were made to the commissural points that verified structural integrity of the single point attached commissures. All single point attached commissures appeared safely anchored at the aortic wall covered with a thin layer of fibrous tissue. The pericardial leaflets remained separated from the base up to the commissural point. In one sheep periannular endocarditis was found with a paravalvular leakage.
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Fig. 4. Autologous pericardial aortic valve prosthesis with single point attached commissures at sacrifice after 11 months.
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Epicardial echocardiography was performed in all sheep intraoperatively after cardiopulmonary bypass. In all 10 sheep, the valves were immediately competent and no remaining regurgitation was recognized (Figs. 5 and 6
). Four out of six sheep had trivial central regurgitation, and one sheep with periannular endocarditis showed a paravalvular leakage with a regurgitation grade III after 6 months. Two out of four sheep had trivial central regurgitation after 11 months.
Instantaneous transvalvular gradient was acquired by inserting a Miller pressure catheter in the ascending aorta and left ventricle after cardiopulmonary bypass, as soon as the circulation was stable and at the time of sacrifice.
The maximum transvalvular gradient immediately after cardiopulmonary bypass was 3.7 ± 2.2 mmHg. At sacrifice the average maximum transvalvular gradient of all sheep was 10.6 ± 5.2 mmHg, with a gradient of 12.5 ± 4.9 mmHg in the sheep sacrificed at 6 months and a gradient of 7.7 ± 4.5 mmHg in the sheep sacrificed at 11 months. The first six sheep had a mean valve size of 22 ± 1.6 mm (4 mm x 21 mm, 1 mm x 23 mm and 1 mm x 25 mm) and the latter four sheep had all a valve size of 21 mm.
5.1 Histology
The specimens stained with hematoxylin/eosin and Masson's trichome showed a normal pericardial tissue with collagen and elastin fibers being intact throughout the entire length of the pericardium. The core of the pericardial tissue appeared acellular. No thrombi present were on the pericardial tissue. The commissures were observed to be intact with a healed attachment to the aortic wall. There was no structural leaflet deterioration and no pericardial tissue calcification or significant inflammation obvious. Masson's trichome stained sections revealed the single point attached commissures anchored to the aortic wall, with the pericardial tissue integrated into the aortic wall and encapsulated by the thick neo-intimal sheath. The basal one-quarter of the ventricular and aortic aspects of the autologous pericardial leaflets was covered with numerous fibroblasts, smooth muscle cells and neointima. No intact epithelial lining was seen at the distal aspects of the pericardial leaflets. Harvested myocardium, liver, spleen, kidney and brain revealed no pathological features, especially no signs of thrombosis.
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6. Discussion
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Since the dawn of cardiac surgery there were several attempts to construct an autologous aortic valve prosthesis [6–10,1]. However, it was Carlos Duran who first introduce a three-dimensional valve mold to construct stentless molded autologous pericardial aortic valve [11,12,1,13]. Although it could be demonstrated by Al Halees et al. [14] that the long-term results of autologous pericardial aortic valve prostheses implanted with the technique introduced by Duran et al. [1] are comparable with commercially available aortic bioprosthesis, the technique was not widely accepted because of the elaborate implantation technique requiring extensive experience and extended surgical time. In order to simplify the construction and implantation of an autologous aortic valve prosthesis, we designed a new generation of stentless autologous pericardial aortic valve prosthesis that combined the principle of valve leaflet molding with the concept of single point attached commissures (SPAC) [4]. The new technique made the construction of a valve prosthesis, that is briefly treated with glutaraldehyde, easy and fast as well as the implantation simple and very reliable.
Theoretically autologous pericardium should experience reduced degeneration because of a non-existing antigenicity. However, experiments with fresh autologous pericardial valve leaflets in the blood stream showed poor results and revealed a very fast shrinkage of the pericardial tissue [15]. It was demonstrated that killing of pericardial cells with ethanol or glutaraldehyde fixation does prevent the accelerated degeneration of living pericardium [15] and is essential if a pericardial leaflet structure is expected to be long-lasting. Although the immunologic response and its effect on long-term durability is not completely understood [16,17], it becomes increasingly clear that autologous pericardium, treated with glutaraldehyde has a good long-term durability in aortic position [18–20]. Al Halees et al. [14] published the largest series of autologous pericardial aortic valve prosthesis in 65 patients with a mean age of 30 years and the longest follow-up of 16 years. It was demonstrated that the behavior and durability of valve prostheses made of pericardium, briefly treated with glutaraldehyde is comparable to commercially available stentless xenografts valve-prosthesis. Al Hallees et al. observed a different mode of valve degeneration in bovine and autologous pericardium. The failed bovine pericardial valves tended to show heavy calcification and extensive fibrosis whereas the autologous pericardium was still pliable with less fibrosis and calcification. This is in line with earlier experiences with stented autologous pericardial valves treated briefly with glutaraldehyde, which disclosed that the autologous pericardium is not prone to calcification but fails because of tears at the connection of the autologous pericardium with the rigid stent [10].
Finite element study, comparing the various geometrical profiles of stentless pericardial valve prosthesis, showed that the three-dimensional molding of valve prosthesis positively influence leaflet stress distribution and coaptation [5]. It can be hypothesized that replicating the three-dimensional shape of the native valve closer to the natural valve will improve long-term durability of autologous pericardial tissue because of reduced stresses magnitudes on the leaflets especially at the commissures, which are leading to structural failure and increase the incident of calcification [21].
By applying the SPAC implantation technique to the molded autologous pericardial valve, the implantation was simplified and the result became exceptionally predictable. All valves were immediately competent even when implanted asymmetrically, and had very low transvalvular gradients. Because of the unique design of this pericardial valve, a competent aortic valve is guaranteed as long as the appropriate size of the valve (according to STJ diameter) was chosen even if the single point attached commissures were implanted asymmetrically [4]. In vitro experiments and finite element analysis revealed an acceptable stress level at the single point attached commissures [4,22,5] and clinical implants proved mid-term durability of SPAC-like valves [23,24]. Our previous experiments showed that the aortic wall is the weakest point of SPAC-valves, which requires reinforcement of the commissural sutures outside of the aorta to prevent the commissural sutures from cutting through the aortic wall [4].
In this series the transvalvular gradient was significantly lower immediately after implantation and cardiopulmonary bypass compared with the transvalvular gradient at sacrifice. We presume that this exceptional low gradient was mainly caused by the depressed hemodynamic and low blood flow after cardiopulmonary bypass, as all valves appeared pliable without stenosis at the time of sacrifice.
In six sheep trace central regurgitation was present at sacrifice. We assumed that the central regurgitation was caused due to the missing noduli arantii that are blocking the central gap in the natural semilunar valves. One sheep was found with a paravalvular leakage because of periannular endocarditis. Sheep with aortic valve replacement are generally known to be prone to endocarditis and pneumonia [25]. Interestingly, Al Halees et al. [14] observed an increased incidence of endocarditis in humans with autologous pericardial aortic valves that were briefly treated with glutaraldehyde. The reason for this observation is not clear, but it is speculated that the reduced toxicity of pericardium that is treated with glutaraldehyde only for a short time, does not prevent endocarditis as effectively as fully tanned pericardium.
In our 11-month-lasting animal trial, the pericardial tissue was only partially covered with an endothelium layer. But it is to be expected that the covering will increase over time as Al Halees et al. [14] found a continuous epithelium-like layer on glutaraldehyde treated autologous pericardial leaflets 16 years after implantation, while the core still remained acellular.
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7. Conclusion
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This new design of a truly stentless aortic valve prosthesis allows fast construction from autologous pericardium and comfortable surgical implantation that can be performed in a standard cross-clamping time. This technique is simple, inexpensive and applicable to all cases of aortic valve disease. The advantages of this stentless molded autologous pericardial aortic valve with SPAC are that:- (1) the valve prosthesis is readily available and cheap;
- (2) the construction of the valve prosthesis is simple and fast;
- (3) the implantation technique is comfortable and save with reliable results;
- (4) the gradient is exceptionally low;
- (5) anticoagulation is not required.
These characteristics of this truly stentless molded autologous aortic valve prosthesis with single point attached commissures make it a valuable alternative, especially for patients with small aortic annulus and contraindication for anticoagulation, and not only in societies where the patients cannot afford to pay for a premanufactured valve prosthesis.
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Acknowledgments
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The authors appreciate the support by Pierce Chow KH PhD, Department of Experimental Surgery, Singapore General Hospital and thank Hou Sen Lim MEng., Bryan Ogden DVM, DACLAM and Robert Ng for their help in performing this research.
The study was performed at Nanyang Technological University, School of Mechanical and Aerospace Engineering Division of Thermal and Fluids Engineering, Singapore.
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Footnotes
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The study was presented as a poster at The Society for Heart Valve Disease Fourth Biennial Meeting, New York, 15–18 June 2007.
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Abstract
1. Introduction
