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Ann Thorac Surg 2000;70:717-722
© 2000 The Society of Thoracic Surgeons

Original articles: cardiovascular

Comparison of porcine xenografts and homografts for pulmonary valve replacement in children

Sven Dittrich, MDa, Vladimir V. Alexi-Meskishvili, MD, PhDb, Abraham C. Yankah, MD, PhDb, Ingo Dähnert, MDa, Rudolf Meyer, MD, PhDc, Roland Hetzer, MD, PhDb, Peter E. Lange, MD, PhDa

a Department of Congenital Heart Disease, Deutsches Herzzentrum Berlin, Berlin, Germany
b Department of Cardiovascular Surgery, Deutsches Herzzentrum Berlin, Berlin, Germany
c Department of Pathology, Deutsches Herzzentrum Berlin, Berlin, Germany

Address reprint requests to Dr Dittrich, Abteilung Angeborene Herzfehler/Kinderkardiologie, Deutsches Herzzentrum Berlin, Augustenburger Platz 1, D-13353 Berlin, Germany
e-mail: svsdittr{at}aol.com


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Due to the limited availability of homografts, different alternatives are used for replacement of the pulmonary valve. This study investigates the value of porcine stentless pulmonary xenografts in pediatric cardiac patients.

Methods. Twenty-three pediatric xenograft (size 10 to 21 mm) recipients were compared with 23 homograft (size 9 to 21 mm) recipients.

Results. Hospital mortality was 2 of 23 patients in the xenograft group and 3 of 23 in the homograft group (NS). Six out of 20 xenografts and 1 of 19 homografts were stenotic after 1 year (p = 0.011). Xenograft stenoses were mainly located at the distal anastomosis, while the leaflets were preserved. Homografts showed valvular stenoses and wall calcification. The 1 year freedom from reoperation was 77% in the xenograft and 93% in homograft recipients (NS), and from transcatheter intervention 84% and 100% (p = 0.004), respectively. Transcatheter intervention in 7 xenograft patients and 1 homograft recipient improved stenosis gradients from 65 to 40 mm Hg (mean) in 6 out of 8 patients. Explanted xenografts showed a loss of elastic membranes and proliferating connective tissue scares coated with activated endothelium.

Conclusions. Xenografts demonstrated a higher incidence of supravalvular obstructions, which were possibly due to unfavorable hemodynamics at the distal anastomosis. Histological findings additionally indicated a pronounced immunological response. Interventional angioplasty lowered the rate of reoperation. Thus, the use of xenografts in children can be accepted as a second choice when a homograft is unavailable.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Homograft valve conduits are used routinely to establish a continuity between the right ventricle and the pulmonary artery [1–4]. In our institution, the pulmonary homograft is favored over the aortic homograft because of better long-term results [5–8]. Nevertheless, early structural deterioration is a frequent problem in infants and children [1, 2, 6, 8, 9]. Moreover, due to heart donor shortage and extended criteria for acceptance, only a limited number of cryopreserved conduits are available, particularly for smaller conduit sizes [1, 10–12]. Therefore, there is great interest in alternatives to homografts. In the past, several valved and non-valved conduits from different materials, eg, pericardium, Dacron (CR Bard, Haverhill, PA), polytetrafluoroethylene, were used to reconstruct the right ventricular outflow tract [10–14]. Though successful pulmonary root replacement with stentless xenografts in infants has been reported after Ross operation [12] and in single pediatric patients [11], the experiences with stentless pulmonary xenografts in the pulmonary position are limited. For this reason, this article evaluates the value of pulmonary root replacements with stentless porcine pulmonary xenografts when compared with pulmonary homografts in pediatric patients.


   Material and methods
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Patients
In our tertiary care center with annually about 350 cardiac open heart operations on congenital heart defects, the standard procedure was pulmonary root replacement with antibiotic-treated and cryopreserved homovital pulmonary homografts as previously described [8, 9]. Since July 1996, all children under 6 years of age were offered Tissuemed glutaraldehyde-treated, freestyle, stentless, pulmonary xenografts (Tissuemed Limited, Swillington, Leeds, UK), if pulmonary root replacement was indicated. Until October 1997, 23 patients received a xenograft in the pulmonary position (Table 1). All parents were informed and gave written consent to pulmonary root replacement with xenograft conduits.


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  		Table 1. Diagnoses and Demographic Dataa

 
A paired control group of 23 patients was retrospectively selected from a historic group of patients, who received a pulmonary root replacement with homografts between January 1994 and October 1997. Controls were matched with respect to diagnoses, body weight, conduit size, and implantation technique (Table 1).

None of the patients in either group received immunosuppressive medication.

Surgical technique
Surgery was performed with bicaval moderate hypothermic (28°C to 32°C) cardiopulmonary bypass and myocardial protection with antegrade crystalloid cardioplegia. Homograft or xenograft size was approximated by adding 2 to 4 mm to the patient’s body surface area normal pulmonary artery valve diameter. Implantation of conduits was performed by the use of the interposition technique, which utilizes 6-0 or 5-0 polypropylene sutures for distal and proximal anastomoses. In patients with hypoplastic main pulmonary arteries or pulmonary bifurcation stenosis, the area was enlarged with autologous pericardium or a polytetrafluorethylene patch followed by distal anastomosis of the homograft or xenograft. Proximal anastomosis to the right ventricle was completed by a hood of autologous pericardium or xenopericardium. The right ventricular to aortic pressure ratio was measured 30 minutes after termination of cardiopulmonary bypass.

Clinical studies
The patient’s charts, operation notes, reoperation data, and repeated echocardiographic data of 6-month intervals were reviewed. Cardiac catheterization was performed when severe graft stenosis or regurgitation was suspected clinically or echocardiographically. Obstruction gradients greater than 50 mm Hg were considered as severe and treated by transcatheter or surgical intervention.

Histology and immunostaining
Explanted homografts and xenografts were evaluated by a pathologist. Specimens were preserved in 8% buffered formaldehyde and paraffin-embedded using standard histological techniques. Slices 5 µm thick were stained with hematoxylin-eosin and elastica van Gieson’s stains. With immunhistological techniques’ myocytes, endothelial cells and macrophages were selectively stained. Antibody binding was visualized by the alkaline phosphatase anti alkaline phosphatase (APAAP) method. All specimens were examined by light microscopy with magnifications from x10 to x400.

Statistics
Statistical analysis was performed by means of the Statistical Package for Social Sciences, using the Student’s t test for comparison of numerical variables between groups. Life tables and the log-rank test were used to reveal significant differences between follow-up graphs. p Values of less than 0.05 were considered to be statistically significant.


   Results
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 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Surgical outcome
In 2 groups with 23 patients each, a porcine xenograft or a homograft was implanted in the pulmonary position (Table 1). In addition, supravalvular pulmonary artery patch enlargement was performed in 6 patients in the xenograft group and 3 patients in the homograft group (Table 2). The right ventricular to aortic pressure ratio revealed no differences between the groups (Table 2). The 2 groups did not differ in terms of hospital mortality, which was 8.7% (2 of 23 patients) in the xenograft group and 12.4% (3 of 23 patients) in the homograft group. There was one late death in the 1st year postoperatively in both groups, 5 and 6 months after surgery, respectively. A 3-year-old boy with pulmonary atresia and ventricular septal defect died of pulmonary complications, and a 7-month-old girl with pulmonary atresia and intact ventricular septum died of causes unknown. Both had shown good graft and right ventricular functions earlier.


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  		Table 2. Operative and Follow-up Dataa

 
Midterm results
At the median follow-up of 2 years after surgery, graft stenosis was found in 66% of the patients with xenograft and in 12% of the patients with homograft implants (p = 0.01). All xenograft obstructions were located at the distal anastomosis site (Fig 1). The homograft patients had stenoses at the valvular site or because of calcified wall obstructions. Two years after surgery, 46% of the patients with xenograft and none of the patients after homograft implants had undergone a transcatheter intervention (Fig 2) (p = 0.048). Freedom from reoperation did not differ between the groups (22% versus 12%, Fig 3). Severe graft valve regurgitation (estimated greater than grade II by color flow mapping) was seen in 3 patients with homografts 37 months (mean) postoperatively, and currently in none of the xenograft patients (Fig 4). Eighty-four percent of the patients in the xenograft group and 90% in the homograft group were available for follow-up. The duration of the follow-up was 24 (range 21 to 31) months in the xenograft group and 40 (range 20 to 63) months in the homograft group (Table 2).



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  		Fig 1. Distal xenograft obstruction caused by intimal proliferation. Porcine pulmonary xenograft (diameter 17 mm) explanted 13 months after reconstruction of the right ventricular outflow tract in an 8 kg, 1-year-old girl with double outlet right ventricle and pulmonary stenosis. Cardiac catheterization before reoperation revealed a systolic pressure gradient of 65 mm Hg between the pulmonary artery and the right ventricle. Chest roentgenogram showed no conduit wall calcification. Replacement of the obstructed xenograft was performed using a non-valved polytetrafluoroethylene graft. (A) View from the proximal anastomosis with a clear image of the well-preserved pulmonary leaflets. (B) View on the distal anastomosis, showing a neointimal peel that caused severe obstruction of the conduit (arrows).

 


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  		Fig 2. Freedom of transcatheter intervention. Absence of graft failure in homograft when compared with xenograft conduits. Indication for transcatheter intervention were valvular or supravalvular transconduit gradients of 50 mm Hg or higher.

 


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  		Fig 3. Freedom of reoperation. Graft survival of homograft versus xenograft conduits before explantation. Obstruction gradients above 50 mm Hg were considered an indication for conduit exchange if untreatable by transcatheter intervention.

 


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  		Fig 4. Freedom of valve incompetence > grade 2. Freedom of valve incompetence (insufficiency > grade II as estimated by color flow mapping) was 65% after 3 years in the homograft group. Xenograft valve function does not differ from homograft valve function within a 2-year follow-up period.

 
Transcatheter interventions
Seven transcatheter interventions were performed 11 ± 7 (mean ± SD) months postoperatively in the xenograft group and one transcatheter intervention was performed 38 months after operation in the homograft group (Fig 2). Transcatheter intervention, performed with balloon dilatation in 5, and with stent implantation in 2, xenograft patients, reduced graft obstruction from {Delta}P 65 to 40 mm Hg (mean) in all but 2 patients (1 explanted and 1 scheduled for explantation). Follow-up time since transcatheter intervention in successfully treated patients was 13 (range 7 to 15) months in the xenograft group, and 25 months for the homograft patients.

Reoperation
Two out of 23 homografts and 4 out of 23 xenografts had to be replaced for severe supravalvular stenosis (Fig 3). Two patients received homografts and 4 patients received valveless polytetrafluoroethylene (TPFE) conduit implants. All survived the reoperation with good results.

Pathology of explanted grafts
The explanted xenografts showed severe distal stenosis due to obstructive neointimal proliferation (Fig 1). Histological examination of the explanted xenografts revealed intact valve tissue and fibrous transformation, which was located in the pulmonary artery wall (Fig 5). The medial layer showed different areas with a loss of elastic membranes. In these areas, the actin filaments had vanished and were replaced by connective tissue scars. Those scarred connective tissue areas consisted of a small number of preexistent smooth muscle cells, single macrophages, and fibroblasts. The supravalvular tissue proliferation created lumen obstruent plaques, which were coated with intact and activated endothelium. Homograft histology revealed a deterioration of the valves with valve retraction and extended calcification of the homograft wall.



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  		Fig 5. Histology of an explanted xenograft. (A) Histological changes in a porcine pulmonary xenograft 13 months after implantation in a 1-year-old patient. The valve tissue appeared intact. In the distal area of the medial layer of the pulmonary artery wall, there is fibrous transformation with loss of elastic membranes. In these areas, the actin filaments have vanished and been replaced by connective tissue scars. (B, C) Larger magnifications. Areas with scar tissue consisted of a small number of preexistent smooth muscle cells, single macrophages, and fibroblasts. The supravalvular tissue proliferation creates an obstruction of the vessel lumen through plaques coated with intact and activated endothelium.

 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
The question as to which conduit should be selected for pediatric patients who have to undergo reconstruction of the right ventricular outflow tract is important clinically [1, 9–11, 14]. While the gold standard homografts are of limited availability [1–4], stentless pulmonary porcine xenografts will always be an available alternative if pulmonary root replacement is indicated [10–12, 14]. However, our investigation of the clinical performance of the two grafts revealed a higher incidence of complications for pediatric xenograft recipients. The major finding was a stenosis at the distal anastomosis site. Our pathological investigation of explanted xenografts after short-term follow-up indicate that a neointimal proliferation at the anastomosis site was involved in the development of these stenoses, while the xenograft valves were unaffected and the xenograft walls showed fibrosis with only minor calcification of the scar tissue during short-term follow-up. The neointimal proliferation can be explained by two mechanisms. First, the freestyle stentless pulmonary xenograft when compared with the homograft is a relatively inflexible and thick vascular conduit. This may cause hemodynamic turbulence at the distal anastomosis site, which could cause intimal injury and secondary intimal proliferation. This hypothesis could explain the occurrence of localized obstruction and is supported by previous reports of a relationship between unfavorable hemodynamic findings of valves or grafts to degeneration [13].

The second explanation is a more pronounced immunological response and rejection of xenografts when compared with homografts, which has previously been shown in animal experiments [15–17]. Additionally, local toxic effects of the glutaraldehyde treatment of the xenografts may have caused damage to the pulmonary artery wall and induced scar formation [16]. Indeed, our histological analysis of explanted xenografts revealed areas with a loss of elastic membranes and missing actin filaments, which were replaced by proliferative connective tissue scars. These scars create lumen-obstructing plaques, which are coated with intact and activated endothelium. The observation of increased proliferative activity in pediatric patients is in line with several previous studies, which have shown a more pronounced immunoreaction, regardless of the allogenic source of the graft in pediatric patients when compared with adults [1, 2, 4, 8, 9, 18]. However, as xenografts did not only show an increased degree of severity but also a different pattern of degeneration, as has been described in homografts [8, 9, 18, 19], early xenograft destruction is clearly not only an issue of extended immunoreactivity in children.

However, the specific type of proliferative distal xenograft stenoses in the absence of severe calcification may be the main reason why, in our experience, the performance of transcatheter angioplasty and stent implantation were appropriate steps to treat distal xenograft obstruction gradients. Thus, the high rate of stenoses in xenografts did not result in more reoperations than in the homograft group.

Limitations of the study
A number of factors, such as Abo-blood group system and human lymphocyte antigen-compatability, and age of the homograft donor, might have influenced the outcome of homografts [8], but could not be considered as meaningful in our small series.

As follow-up is shorter in xenografts, the question of whether xenografts, which do not have the problem of distal stenosis or in which distal obstructions have been sufficiently treated, will develop valve degeneration and wall calcification as in homografts remains open to future investigation. Recently, Schoof and colleagues [16] demonstrated unfavorable results for the Medtronic freestyle stentless aortic xenograft (Medtronic, Düsseldorf, Germany) in the pulmonary position in growing pigs. They found severe destruction due to inflammatory changes in the xenografts with severe valvular stenosis and graft failure similar to the frequently described homograft degeneration [8, 9, 18, 19].

Conclusion
The glutaraldehyde-treated Tissuemed porcine stentless pulmonary xenograft can be used as a second choice therapy in pediatric patients who have to undergo right ventricular outflow tract reconstruction with an acceptable short-term morbidity and mortality if a pulmonary homograft is unavailable. The major disadvantage of porcine pulmonary xenografts is a high rate of distal anastomosis stenoses, which may be due to unfavorable hemodynamics as a result of stiff material and to extended tissue proliferation tendencies in children. Early distal xenograft stenoses can be successfully treated by transcatheter angioplasty and stent implantation, thus keeping the explantation rate during short-term follow-up comparable with homografts.


   Footnotes
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 Footnotes
Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/section/atsdiscussion/


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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  5. Bando K., Danielson G.K., Schaff H.V., Mair D.D., Julsrud P.R., Puga F.J. Outcome of pulmonary and aortic homografts for right ventricular outflow tract reconstruction. J Thorac Cardiovasc Surg 1995;109:509-517.[Abstract/Free Full Text]
  6. Stark J., Bull C., Stajevic M., Jothi M., Elliott M., de Leval M. Fate of subpulmonary homograft conduits. J Thorac Cardiovasc Surg 1998;115:506-514.[Abstract/Free Full Text]
  7. Weipert J., Meisner H., Mendler N., et al. Allograft implantation in pediatric cardiac surgery. Ann Thorac Surg 1995;60:S101-S104.
  8. Schorn K., Yankah A.C., Alexi-Meskhishvili V., Weng Y., Lange P.E., Hetzer R. Risk factors for early degeneration of allografts in pulmonary circulation. Eur J Cardiothorac Surg 1997;11:62-69.[Abstract]
  9. Yankah A.C., Alexi-Meskhishvili V., Weng Y., Schorn K., Lange P.E., Hetzer R. Accelerated degeneration of allografts in the first two years of life. Ann Thorac Surg 1995;60:S71-S76.
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  11. Kleikamp G., Breymann T., Thies W.R., et al. Stentless xenograft valve in a truncus arteriosus communis. Ann Thorac Surg 1993;56:1171-1172.[Abstract]
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  13. Agarwal K.C., Edwards W.D., Feldt R.H., Danielson G.K., Puga F.J., McGoon D.C. Pathogenesis of nonobstructive fibrous peels in right-sided porcine-valved extracardiac conduits. J Thorac Cardiovasc Surg 1982;83:584-589.[Abstract]
  14. Champsaur G., Robin J., Curtil A., et al. Long-term clinical and hemodynamic evaluation of porcine valved conduits implanted from the right ventricle to the pulmonary artery. J Thorac Cardiovasc Surg 1998;116:793-804.[Abstract/Free Full Text]
  15. Heinzerling R., Stein P., Riddle J., Magilligan D., Jr, Jennings J. Immunological involvement in porcine bioprosthetic valve degeneration. Henry Ford Hosp Med J 1982;30:146-151.[Medline]
  16. Schoof P.H., Hazekamp M.G., van Krieken H.H., Huysmans H.A. Pulmonary root replacement with the freestyle stentless aortic xenograft in growing pigs. Ann Thorac Surg 1998;65:1726-1729.[Abstract/Free Full Text]
  17. Yankah A., Wottge H. Allograft conduit wall calcification in a model of chronic arterial graft rejection. J Card Surg 1997;12:86-92.[Medline]
  18. Baskett R.J., Ross D.B., Nanton M.A., Murphy D.A. Factors in the early failure of cryopreserved homograft pulmonary valves in children. J Thorac Cardiovasc Surg 1996;112:1170-1178.[Abstract/Free Full Text]
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Accepted for publication March 31, 2000.


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B. Aupecle, A. Serraf, E. Belli, S. Mohammadi, F. Lacour-Gayet, P. Fornes, and C. Planche
Intermediate follow-up of a composite stentless porcine valved conduit of bovine pericardium in the pulmonary circulation
Ann. Thorac. Surg., July 1, 2002; 74(1): 127 - 132.
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K. R. Kanter, J. M. Budde, W. J. Parks, V. K.H. Tam, S. Sharma, W. H. Williams, and D. A. Fyfe
One hundred pulmonary valve replacements in children after relief of right ventricular outflow tract obstruction
Ann. Thorac. Surg., June 1, 2002; 73(6): 1801 - 1807.
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S. Saito
Replacement of the iliac vein: reply
Ann. Thorac. Surg., May 1, 2002; 73(5): 1692 - 1692.
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