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Ann Thorac Surg 2005;80:969-975
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Advances in Experimental Percutaneous Pulmonary Valve Replacement

Tim Attmann, MD a , Thomas Jahnke, MD b , René Quaden, MD a , Andreas Boening, MD, PhD a , Stefan Muller-Hulsbeck, MD, PhD b , Jochen Cremer, MD, PhD a , Georg Lutter, MD, PhD a , *

a Department of Cardiovascular Surgery, Christian-Albrechts-University of Kiel, School of Medicine, Kiel, Germany
b Department of Radiology, Christian-Albrechts-University of Kiel, School of Medicine, Kiel, Germany

Accepted for publication March 8, 2005.

* Address reprint requests to Dr Lutter, Department of Cardiovascular Surgery, Christian-Albrechts-University of Kiel, School of Medicine, Arnold-Heller-Str 7, 24105 Kiel, Germany (Email: lutter{at}kielheart.uni-kiel.de).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Percutaneous pulmonary valve implantation is emerging as an alternative and additional option for a successful surgical scheme. To date, these procedures are performed by the balloon-in-balloon technique. The use of self-expanding stents for percutaneous valve replacement is assumed to improve preservation of the valve in its folded condition in the application device and the valve’s long-term functioning. Therefore, initial experience with the development of a completely percutaneous transfemoral technique for pulmonary valve implantation using a self-expanding valved stent is described.

METHODS: Bovine jugular xenografts were sutured into nitinol stents, and functional in vitro tests of valved stents were carried out. Transfemoral implantation in pulmonary position was acutely evaluated in 6 sheep weighing 22 to 29 kg. Radiologic evaluation was performed by angiography and multislice computed tomography (MSCT) scan. In addition, pathoanatomical studies were performed.

RESULTS: Exact implantation in pulmonary valve position was achieved in 5 of 6 sheep, with 1 early stent migration. Another sheep died before stent placement owing to perforation of the right ventricle by the delivery system. Orthotopic pulmonary valved stent position was depicted by MSCT in all other sheep (n = 4). The peak-to-peak transvalvular gradient was 8.2 ± 3.9 mm Hg (n = 5). Postmortem examination revealed intact stent valves with no adherent clots. No macroscopic damage of the pulmonary artery was noted, whereas minor hematoma of the right atrium and the right ventricular outflow tract were observed in 2 hearts.

CONCLUSIONS: This acute study demonstrates that memory nitinol valved stents can be optimally deployed in the pulmonary position through the groin in sheep.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Patients having undergone surgery for congenital heart disease are often candidates for reoperations. In particular, pulmonary regurgitation can occur after operative corrections of the right ventricle, its outflow tract (RVOT), and the pulmonary artery. Percutaneous pulmonary valve implantation is emerging as an alternative or additional option for a successful surgical scheme, recently even being introduced into clinical practice. The procedures described were performed by the balloon-in-balloon technique [1].

In contrast, the use of self-expanding stents for percutaneous valve replacement is assumed to improve preservation of the valve in its folded condition in the application device and the valve’s long-term functioning. Furthermore, the implanting procedure of self-expanding stents might have hemodynamic advantages because the balloon does not occlude the outflow tract [2]. However, this potential problem has not become apparent in clinical studies [1, 3].

We report our initial experience with this development of a totally percutaneous transfemoral technique for pulmonary valve implantation in an ovine model using self-expanding stents. The aim of the study was to show the feasibility of this kind of stent-implantation. In addition, functional and patho-anatomical parameters were assessed.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Stent Design
Radially self-expanding nitinol stents (Nitinol Devices & Components, Fremont, California) were used in the present study. The stent wires are soft and highly malleable, molding two ranks of 14 rhombs each. Bare stents were 28 mm in length and 22 or 24 mm in diameter when fully expanded.

Preparation of Valved Stents
The basic principles of using a bovine jugular vein for valved stent production were described by Khambadkone and Bonhoeffer [4]. Bovine jugular veins were acquired from a local abattoir. Segments containing bicuspid or tricuspid native valves were carefully prepared and the external wall thinned. After preservation with glutaraldehyde, the valved vein segments were sutured to the interior of the nitinol stents with 7–0 polypropylene sutures (Fig 1).



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  		Fig 1. Valved segment of a bovine jugular vein inside the nitinol stent: (a) during suturing process and (b) view from above on a bicuspid valve with thin, transparent cusps.

 
In Vitro Tests
In the pulsatile flow simulation, the function of the stent valves and transvalvular pressure conditions were assessed. Opening, closure, and movement of the leaflets were captured with an endoscope suspended above the valve in the fluid stream. Use of dispersion particles allowed the determination of laminar or turbulent flow.

Animal Model and Implantation Procedure
Six consecutive studies in sheep weighing 22 to 29 kg are reported. Animals received humane care in accordance with the "Principles of Laboratory Animal Care" and the "Guide for the Care and Use of Laboratory Animals" (National Institutes of Health publication 85–23, revised 1985). A committee on animal research at Kiel University approved the protocol. After premedication with intramuscular ketamine, midazolam, and atropine, an ear vein was cannulated and endotracheal intubation was performed. General anesthesia was maintained with continuous infusion of propofol and ketamine boli. Ringer’s solution served as a volume substitute. The animals were mechanically ventilated, positioned on an angiography suite table in supine position, and continuously electrocardiographic monitored.

A 5F sheath was placed in the left femoral artery for continuous blood pressure monitoring and repetitive blood gas analyses. Both femoral veins were instrumented with 9F sheaths for the introduction of an angiographic catheter as well as a calibrated marker catheter.

After angiographic assessment of the pulmonary artery, an extra-stiff, soft-tipped 0.035-inch guidewire was advanced in the left pulmonary artery through the sheath in the right groin. After heparin (200 IU/kg) was administered, the right 9F sheath was replaced by a 24F sheath.

The valved stent was hand crimped and inserted into a modified commercially- available application device (22F outer diameter), which was advanced over the guidewire into pulmonary position. The size of the stent chosen was dependent on the diameter of the pulmonary annulus measured by angiography after calibrating of the intrinsic measuring system of the angiography unit. Positioning of the application device was controlled fluoroscopically using digital image overlay. The self-expanding valved stent was slowly deployed directly over the native pulmonary valve and immediately took over its function. After deployment, the application device was carefully retrieved and heparin was antagonized by protamin. Completion angiography and transvalvular pressure measurements followed (Micro-Tip Millar Catheter; Millar Instruments, Houston, Texas). The 24F sheath was removed and after manual compression for 20 minutes, the skin in the right groin was closed with a single stitch. The animals were transferred to the CT laboratory (Sensation 16; Siemens, Erlangen, Germany) and a contrast-enhanced CT scan was carried out. After the imaging studies, the sheep were sacrificed in deep anesthesia with a high intravenous dose of potassium chloride.

Graft Retrieval and Pathoanatomical Study
At postmortem, the right ventricle was opened horizontally 3 cm from the apex, and the RVOT and the pulmonary artery were opened longitudinally for evaluation of valved stent positioning. All stent valves were explanted, and macropathology studies were carried out. The atrial and ventricular chambers and the inferior vena cava were exposed to look for catheter-induced damage.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
In Vitro Studies
Valves promptly opened and closed. The thin leaflets exhibited no resistance; there was a low transvalvular pressure gradient of 5.2 ± 1.8 mm Hg on average in 6 valves. Laminar flow was recorded in all valves. Minor turbulence was found in 3 of 6 stent valves (Fig 2).



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  		Fig 2. Endoscopic view from above on a valved stent in the in vitro pulsatile flow system: (a) prompt and wide opening of the cusps during systole and (b) complete closure during diastole.

 
In Vivo Studies
The mean diameter of the pulmonary annuli was 20.1 mm (range, 18.5 to 20.5 mm) as revealed by angiography (Fig 3). Valved stents with a maximal outer diameter from 18.8 to 23.5 mm were used. Mean duration of the procedure from insertion of the application device through the sheath to deployment was 37.8 seconds (range, 13.9 to 68.0). The fluoroscopy time of the entire procedure (n = 5) ranged from 7.4 to 10.7 minutes (mean 8.4).



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  		Fig 3. Preimplantation angiography of the right ventricular outflow tract and the pulmonary artery. The annulus is 20.3 mm. Note: there is little contrast agent in the right atrium (arrow).

 
One of the 6 sheep died before stent placement owing to perforation of the right ventricle by the delivery system. In the remaining 5 animals, the valved stents were deployed correctly at the target site over the native pulmonary valve. After initial orthotopic positioning, CT scan detected early stent migration in 1 animal. Orthotopic pulmonary valved stent position (n = 4) was depicted by CT in all other sheep (Fig 4).



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  		Fig 4. Three-dimensional computed tomography reconstructions of the heart in volume rendering technique modus after implantation of a valved stent in the pulmonary position. Spin degrees: –22 for the left upper picture, +23 for the left lower picture, +68 for the right upper picture, and +90 for the right lower picture.

 
Valves were angiographically and hemodynamically competent (Fig 5). No paravalvular leakage could be detected by angiography. The implanted valved stents (n = 5) showed a low transvalvular gradient of 8.2 ± 3.9 mm Hg on average (peak-to-peak; Fig 6).



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  		Fig 5. Completion angiography after valved stent deployment. No neovalve insufficiency is detected.

 


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  		Fig 6. Typical shape of pressure curves during catheter pullback through the valved stent.

 
An alteration of the geometry of cardiac structures induced by the extra-stiff guidewire and especially by the application device was registered by angiography (Fig 7). During the deployment procedure, rhythm disturbances occurred in all animals, and mean arterial blood pressure dropped from 84.4 ± 24.0 mm Hg to 71.0 ± 30.4 mm Hg. Five minutes after deployment, mean arterial blood pressure recovered to 75.3 ± 27.6 mm Hg (n = 5).



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  		Fig 7. Fluoroscopy with application device in situ. Note the alteration of the geometry of cardiac structures induced by the extra-stiff guidewire and by the application device. The black arrow indicates the position of the pulmonary annulus before introduction of the guide wire and the application device. The white arrow indicates the new position of the pulmonary annulus.

 
Pathoanatomical Study
Postmortem examination confirmed the correct position of the valved stents in 4 sheep (Fig 8a). In 1 animal, the valved stent was found in the pulmonary artery approximately 1 cm distal to the pulmonary valve as already depicted in CT. The neovalve leaflets were thin and perfectly mobile with no adherent clots (Fig 8b). After rinsing with water, valves showed no insufficiency. The cusps of the native pulmonary valve were squeezed between the stent and the pulmonary wall, being fully inoperable. The stent’s high radial expansion capacity was shown by the imprint on the pulmonary intima (Fig 8c). No macroscopic damage of the pulmonary artery was noted, whereas minor hematoma of the right atrium and the RVOT were observed in 2 hearts. There were no coagula in the vicinity of the stents neither in the RVOT nor in the pulmonary artery.



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  		Fig 8. (a) Perfect position of the valved stent. The right ventricular outflow tract and pulmonary artery are cut longitudinally. The arrow indicates a native pulmonary valve leaflet. (b) Valved stent after explantation. Note the thin and transparent leaflets. The small defect (arrow) disappeared during water rinse testing. (c) Imprint of the valved stent on the native pulmonary valve and on the intima of the right ventricular outflow tract and pulmonary trunk. Minor endocardial lesions of the right ventricle are indicated by the arrow.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Right heart failure, sudden death, and arrhythmias due to ongoing pulmonary regurgitation are recognized as the main dilemmas after congenital heart disease surgery. Pulmonary valve replacement is considered when the clinical status of patients is worsening with signs of right ventricular dysfunction. Surgical pulmonary valve replacement is associated with low morbitity and mortality; however, reoperations during mid- and long-term follow-up are very common. The risk of extracorporeal circulation, infection, and also special reoperation risks remain [5]. Furthermore, the adequate timing for pulmonary valve insertion is discussed controversially [6]. An increasing adult congenital heart patient population affected by this issue might benefit from less invasive methods for the correction of the pulmonary valve and the neighboring structures. Only a few groups have undertaken efforts for the development of truly minimally invasive pulmonary valve replacement [7].

Corno and coworkers [7] transventricularly implanted self-expanding valved stents in the pulmonary position of pigs. They demonstrated that off-bypass implantation is feasible with adequate hemodynamic function [7], and the major advantage of this procedure is its suitability independent of body weight and height. Therefore, it is principally even suited for little children. In contrast, the theoretic advantages of percutaneous endoluminal pulmonary valve replacement compared with the surgical procedure are well known [8]. However, catheter-based techniques are limited by the mismatch between the size of the femoral vessels of small children and the application devices. Nevertheless, both approaches could reduce the risks of operations with extracorporeal circulation.

Another scenario in which pulmonary valve operations become necessary are stenoses of biological valved conduits implanted during repair of complex congenital heart defects [9]. The minimal invasive approach to this affliction with self-expanding stents requires a preceding balloon dilation of the calcified conduit structures because the expansion force of the stent might not be high enough to reach a sufficient valve area. However, a dilation procedure can lead to embolic complications, paravalvular leakage, hemorrhage, and a smaller valve area compared with a surgical procedure [10, 11]. Our group is working on an alternative procedure for the solution of these problems: percutaneous valve resection. In a preliminary study, the use and feasibility of a high-pressure water jet system as a new promising surgical method for the endovascular ablation of human calcified aortic valves has been successfully performed and evaluated [12]. One might dare to consider transferring this system developed for the left heart to the right heart’s morphology.

The need for the implementation of this idea should be discussed among those who are adept in this emerging field of percutaneous pulmonary valve interventions. In any case, the realization of an ideal endoluminal valve replacement process is challenging, and only sophisticated technical refinements of the tools will lead to success [11, 12].

Bonhoeffer and coworkers are surely at the forefront and represent the leading group in the subject area of percutaneous pulmonary valved stent implantation. Their recently reported human pulmonary valve program is unparalleled [11]. In their animal model, they chose a jugular approach. In contrast, we demonstrated that a nonsurgical transfemoral approach in young sheep is also possible. The 24F sheath was introduced and retrieved with utmost caution, and manual compression of the right groin allowed the inguinal approach. The experience we gained at our center in endovascular aortic stent grafting for the exclusion of thoracic and abdominal aneurysms was useful for the handling of large introducer sheaths and self-expanding stents [13].

Balloon-expandable stents deployed in the great vessels near the heart are prone to dislocation as a result of ongoing mechanical movements and retraction of the surrounding tissue. The continuously exerted radial force of self-expanding stents and their high flexibility assure a geometric adaption to anatomical and tissue-property changes. Furthermore, the mechanical forces to the contacting tissue are equally distributed. Balloon-expandable stents at least have a three times higher radial stiffness compared with identically designed self-expanding stents, namely, a balloon-expandable stent will significantly decrease the compliance of the stented vessel [14].

In our study, an oversizing of approximately 20% proved to be sufficient for secure anchoring. One early stent migration occurred, in which the valved stent’s diameter was only about 12% larger than the size of the pulmonary trunk.

Others have implemented a long-term animal model for pulmonary valve implantation with a survival of 2 months using balloon-expandable stent valves [8]. For the evaluation of late migration and function of self-expanding valved stents, such long-term studies should also follow.

Evolution of the stent design might make this technique suitable for more patients with a more complex anatomy of the RVOT. Boudjemline and colleagues [15] designed a device for infundibular reduction that is very promising. An ideal pulmonary valved stent may be achieved for long-term use by individually lining the RVOT and pulmonary trunk [16].

The drop in blood pressure observed during deployment can be explained by the deformation of the right heart structures by the application device (Fig 7). This deformation is pronounced and could result in damage of the myocardium or the tricuspid valve. We observed minor hematoma of the RVOT in two animals. Furthermore, in the first animal of the study, perforation of the right ventricle occurred. With growing experience, this complication could be ruled out. Further refinement of the application device may prevent damages to cardiac structures.

Limitations
Naturally, short-term experiments cannot provide information about the durability of the biological valve in the stent, the reaction of the surrounding tissue, or the possibility of a delayed stent migration. Bovine jugular veins have a limited maximal diameter of approximately 24 mm. Therefore, they are not suitable for an enlarged RVOT or pulmonary trunk.

In conclusion, this study proves the feasibility of completely percutaneous transfemoral implantation of self-expanding valved stents in the pulmonary position of sheep.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
Doctor Lutter’s project of percutaneous valve replacement is supported by the German Research Foundation (Grant LU 663/4-1, LU 663/4-2). We thank Marion Frahm, Kristin Rumberg, Beata Hoffmann, Andreas Bohlen, Philip Haaf, Christian König, Florian Alten, and Thilo Schulte for their technical and operative assistance. Gerd Pfister and Martin Steiner (Institute of Physics, University of Kiel) have contributed to the in vitro tests.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Bonhoeffer P, Boudjemline Y, Qureshi SA, et al. Percutaneous insertion of the pulmonary valve J Am Coll Cardiol 2002;39:1664-1669.[Abstract/Free Full Text]
  2. Ferrari M, Figulla HR, Schlosser M, et al. Transarterial aortic valve replacement with a self expanding stent in pigs Heart 2004;90:1326-1331.[Abstract/Free Full Text]
  3. Cribier A, Eltchaninoff H, Tron C, et al. Early experience with percutaneous transcatheter implantation of heart valve prosthesis for the treatment of end-stage inoperable patients with calcific aortic stenosis J Am Coll Cardiol 2004;43:698-703.[Abstract/Free Full Text]
  4. Khambadkone S, Bonhoeffer P. Percutaneous implantation of pulmonary valves Expert Rev Cardiovasc Ther 2003;1:541-548.[Medline]
  5. Kanter KR, Budde JM, Parks WJ, et al. One hundred pulmonary valve replacements in children after relief of right ventricular outflow tract obstruction Ann Thorac Surg 2002;73:1801-1806.[Abstract/Free Full Text]
  6. Therrien J, Siu SC, McLaughlin PR, Liu PP, Williams WG, Webb GD. Pulmonary valve replacement in adults late after repair of tetralogy of fallotare we operating too late?. J Am Coll Cardiol 2000;36:1670-1675.[Abstract/Free Full Text]
  7. Zhou JQ, Corno AF, Huber CH, Tozzi P, von Segesser LK. Self-expandable valved stent of large sizeoff-bypass implantation in pulmonary position. Eur J Cardiothorac Surg 2003;24:212-216.[Abstract/Free Full Text]
  8. Bonhoeffer P, Boudjemline Y, Saliba Z, et al. Transcatheter implantation of a bovine valve in pulmonary position. A lamb study Circulation 2000;102:813-816.[Abstract/Free Full Text]
  9. Boethig D, Thies WR, Hecker H, Breymann T. Mid term course after pediatric right ventricular outflow tract reconstructiona comparison of homografts, porcine xenografts and Contegras. Eur J Cardiothorac Surg 2005;27:58-66.[Abstract/Free Full Text]
  10. Robicsek F, Harbold Jr NB, Daugherty HK, et al. Balloon valvuloplasty in calcified aortic stenosisa cause for caution and alarm. Ann Thorac Surg 1988;45:515-525.[Abstract]
  11. Lutter G, Ardehali R, Cremer J, Bonhoeffer P. Percutaneous valve replacement current state and future prospects Ann Thorac Surg 2004;78:2199-2206.[Abstract/Free Full Text]
  12. Quaden R, Attmann T, Böning A, Cremer J, Lutter G. Percutaneous aortic valve replacementresection before implantation. Eur J Cardiothorac Surg 2005;27:836-840.[Abstract/Free Full Text]
  13. Brandt M, Hussel K, Walluscheck KP, et al. Stent-graft repair versus open surgery for the descending aortaa case-control study. J Endovasc Ther 2004;11:535-538.[Medline]
  14. Duerig TW, Wholey M. A comparison of balloon- and self-expanding stents Min Invas Ther Allied Technol 2002;11:173-178.
  15. Boudjemline Y, Agnoletti G, Bonnet D, Sidi D, Bonhoeffer P. Percutaneous pulmonary valve replacement in a large right ventricular outflow tractan experimental study. J Am Coll Cardiol 2004;43:1082-1087.[Abstract/Free Full Text]
  16. Lutter G, Kuklinski D, Berg G, et al. Percutaneous aortic valve replacement: an experimental study. I. Studies on implantation J Thorac Cardiovasc Surg 2002;123:768-776.[Abstract/Free Full Text]



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