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Eur J Cardiothorac Surg 2003;23:560-566
© 2003 Elsevier Science NL

Homograft replacement of the mitral valve in young recipients: mid-term results

S. Chauvauda*, T. Waldmanna, N. d'Attellisb, P. Brunevalc, C. Acard, J. Gerotae, M. Jarrayae, A. Carpentiera

a Department of Cardiovascular Surgery, Hôpital Européen Georges Pompidou, 20, rue Leblanc, 75015 Paris, France
b Department of Anesthesiology, Hôpital Européen Georges Pompidou, 20, rue Leblanc, 75015 Paris, France
c Department of Anatomopathology, Hôpital Européen Georges Pompidou, 20, rue Leblanc, 75015 Paris, France
d Department of Cardiac Surgery, Hôpital Pitié Salpetrière, 47/83 Boulevard de l'Hôpital, 75013 Paris, France
e Human Tissue Bank Hôpital Saint Louis, 1 avenue Claude Vellefaux, 75010 Paris, France

Received 24 September 2002; received in revised form 24 December 2002; accepted 29 December 2002.

* Corresponding author. Tel.: +33-1-56-09-36-26; fax: +33-1-56-09-22-19
e-mail: sylvain.chauvaud{at}egp.ap-hop-paris.fr


   Abstract
Top
 Abstract
1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
Objective: Mitral homograft (MH) can represent an interesting alternative for valve replacement in the young. However, concerns have been expressed about the durability of valve allografts in children. We report our experience with MH replacement in young patients. Methods: From 1993 to 1997, 13 young patients aged 3–25 years (mean 15±6 years) underwent total mitral valve (MV) replacement with a cryopreserved homograft (CH). All but one had previously undergone one or more cardiac operations. The indications were rheumatic disease (6), acute and subacute endocarditis (2), congenital heart disease (4), and systemic lupus endocarditis (1). Results: No in hospital deaths are reported. Discharge echocardiogram showed a well-functioning MH in all but one patient. One patient was lost to follow-up. Follow-up ranged from 0.7 to 6.6 years (4.1±2.2). On follow-up two patients were doing well. Two patients died without reoperation and both had MV stenosis. Seven patients (54%) required reoperation: mean delay 4.17 years (0.7–7). In all cases, thickening, shrinking and calcification of the allograft were present. None of these seven had contributive histopathologic changes. One patient presenting recurent MV insufficiency will require a reoperation. Conclusion: MV homograft is a safe and reproducible technique, but does not provide durable results and should not be used in young patients.

Key Words: Mitral valve homograft • Mitral valve reconstruction


   1. Introduction
Top
 Abstract
 1. Introduction
2. Material and methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
Homograft valves are largely used in children as a conduit between the right ventricle and the pulmonary arteries with various results [1]. Aortic valve homografts are routinely used in aortic position even in children [2,3]. Due to the poor results of bioprosthesis and mechanichal prosthesis in the mitral position in young patients, a mitral homograft (MH) was thought to be an ‘interesting’ alternative technique when conservative surgery was not possible [4].

In our current study we review our series from the beginning of our experience. The aim of this study was to analyze mid-term durability of this valve substitute in young patients.


   2. Material and methods
Top
 Abstract
 1. Introduction
 2. Material and methods
3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
2.1. Patient population
Between 1993 and 1997, 13 patients less than 25 years old (range 3–25) underwent total mitral valve (MV) replacement with homograft (Table 1). Indication for surgery was MV insufficiency in all cases with functional class (New York Heart Association, NYHA) III and IV. All patients were in sinus rhythm, mean cardiothoracic ratio was 0.58±0.08 (range 0.50–0.75).


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  		Table 1. Patient characteristicsa

 
Etiologies were rheumatic disease (6), congenital atrio-ventricular defect (4) (partial (1), total (1), double discordance (1), isolated congenital MV insufficiency (1)), bacterial endocarditis (2) (one acute, one sterile), and systhemic lupus erythematosus (SLE) (1). All patients except one had at least one attempt of a MV repair. Mean delay between the last operation and the replacement with a MH was 4.1±4 years (range 0.4–13.2). One patient had two implantations of a MH. The first attempt was not technically satisfactory leading to early reoperation (patient 13).

Associated procedures were: tricuspid valve annuloplasty (2), tricuspid valve commissurotomy (1), tricuspid valve replacement with a MH (1), aortic valve homograft (1), and closure of atrial septal defect (1).

2.2. Homograft implantation
In all cases a cryopreserved MV obtained from a tissue bank (Banque de Tissus de l'AP-HP) was used. Harvesting of MVs was from two origins. In multiorgan donors, (n=6) the heart was placed in lactated Ringer solution at 4°C. The dissection of the valves was performed as soon as possible. The valves were stored in RPMI solution for 24 h with antibiotics (vancomycin 500 mg/l, lincomycin 600 mg/l and gentamycin 320 mg/l). Afterwards, cryopreservation was started in a medium containing RPMI, human albumin (1.3%) and dimethyl sulfoxide (10%). In living patients (n=7) scheduled for heart transplant, the heart was explanted and stored in lactated Ringer solution at 4°C. The valves were dissected as soon as possible and cryopreservation was started. In this group, the heart was not stored in an antibiotic solution. The mean delay between harvesting and cryopreservation was 26 h.

The operative technique performed was that described by Acar et al. [4] without modifications. All patients except one (patient 6) had a Carpentier prosthetic ring.

Homograft characteristics are listed in Table 2. Blood groups of both recipient and donor are presented in Table 3. Matching of blood groups was not attempted.


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  		Table 2. Homograft characteristics

 

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  		Table 3. Blood groups, rhesus and evolution of the homografta

 
Cardiopulmonary bypass was performed at a core temperature of 28°C, with cold blood cardioplegia. Average bypass time was 158±34 min (120–120) and aortic cross-clamping 103±19 min (80–140).

2.3. Statistical analysis
Continuous or interval-related variables are expressed as means±SD and categoric variables are expressed as percentage. Events were calculated by the Kaplan–Meier actuarial method.


   3. Results
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
4. Discussion
 Appendix A. Conference...
 References
 
3.1. Early results
No in hospital deaths are reported following MV homograft implantation. A control transesophageal echocardiography was performed in the operating room and before hospital discharge (tenth postoperative day). All patients except one (patient 13), were free of MV stenosis (Table 4). MV insufficiency was graded from 1+ to 4+. Residual MV insufficiency graded 2+ was present in three patients, but clinically well tolerated. Cyclosporin (serum level 80 ng/ml) and aspirin 50 mg per day were administered in one patient (patient 11).


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  		Table 4. Echocardiographic results: early and late evaluation correlated with the clinical outcomea

 
3.2. Follow-up
One patient was lost to follow-up. Mean follow-up with clinical examination and echocardiography was 4±2.2 years (min 0.7, max 7). Patient follow-up was stopped when the MV was replaced.

3.3. Clinical evolution
At the last follow-up, two patients were doing well with no sign of homograft dysfunction (patients 4 and 9). One patient presented massive MV homograft insufficiency and was scheduled for valve replacement. Two patients died and had MV stenosis. One of these patients had global cardiac failure and was not reoperated for geographic reasons. The other patient died of multiple causes: SLE, renal insufficiency and probable recurrent bacterial endocarditis. Seven patients were reoperated on for MV homograft dysfunction.

Out of seven patients with incompatible patient/homograft blood groups, six had valve failure (reoperated on or not). Out of six patients with compatible patient/homograft blood groups, four had valve failure (reoperated on or not) (Table 3). The difference between the two groups was not significant.

3.4. Reoperation
Seven patients underwent MV replacement, with a mechanical bileaflet valve (6) or bioprosthesis (1), without complication. The smallest diameter of the prosthesis implanted was 25 mm.

Indications for replacements were massive MV insufficiency (3) or stenosis (4) (Table 4). Active endocarditis was present in one patient and degeneration in six patients.

Clinical examination of the degenerated homograft during surgery revealed obstructive calcification (3), chordal rupture (1), valve retraction with an inflammatory aspect (2).

The actuarial freedom from reoperation is 43±16% at 5 years and 30±16% at 7 years (Fig. 1 ). The actuarial freedom from valve failure (association of reoperation and dysfunction) was 30±14% at 5 years and 12±10% at 7 years (Fig. 1b).



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  		Fig. 1. Actuarial rate of complications (Kaplan–Meier). (a) Freedom from reoperation. (b) Freedom from complication combining reoperation and mitral dysfunction (without reoperation).

 
3.5. Pathology of explanted valves
Five explanted valves underwent microscopic examination. The papillary muscles appeared to be fibrotic in all cases and in one, necrosis was present. Absence of leaflet tissue endothelium was encountered in all explanted valve. Massive fibrosis of the stroma was at the origin of a total disorganization of the leaflet structure. The fibrosa and the spongiosa were totally replaced by fibrosis in most cases with hemorrhage in the stroma (Fig. 2a ). Intense neovascularization was present in one specimen, (Fig. 2b) on the leaflet and on the chordae (patient 8). Calcification was present with ulcerated plaques (Fig. 2c) (patients 11 and 13) associated with thrombosis (Fig. 2d). The inflammatory cells when present were non-specific: lymphocytes B and macrophages (Fig. 3 and Table 5).



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  		Fig. 2. Histologic changes of the stroma. Hematoxylin and eosin stain. (a) Hemorrhage associated with fibrosis (original magnificationx100). (b) Subendothelial leaflet calcification (original magnificationx100). (c) Inflammatory cells, most of them are macrophages (original magnificationx50). (d) Neovascularization with extensive fibrosis (original magnificationx50).

 


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  		Fig. 3. Histologic changes of the endothelium. Thrombosis adherant to the leaflet tissue and absence of endothelium cells, the stroma is highly fibrotic. Hematoxylin and eosin stain (original magnificationx50).

 

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  		Table 5. Pathology of the explanted valves

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
Appendix A. Conference...
 References
 
Following the ‘acceptable’ clinical experience of aortic homograft in young patients [5] it was assumed that MV homograft replacement could be used in children [6]. However, it is known that degeneration of aortic homografts is related to the young age of the recipient [7] with a predominance of inflammatory lesions [8]. Clinical mid-term results of MHs are rare. In Acar et al.'s [4] study, mean follow-up was 14 months with a very low rate of reoperation and residual MV insufficiency. In contrast, the series of Kumar et al. [9] is less favorable; the actuarial rate of normal function was 42 and 10% at 24 and 48 months, respectively. In the series by Doty and Acar [10], 25% (5/18) of the MHs was explanted during the first postoperative year despite the accuracy of the repair confirmed by intraoperative echocardiography. Patients operated on in poor clinical condition had good early results, but proved to evolve toward mid-term failure [11].

When considering the high incidence of failure in our series we attempted to analyze and understand the causes.

4.1. Surgical technique
In our series we performed a side to side suture of the papillary muscle [4] and no rupture of papillary muscle occurred. This complication which can occur irrespective of the age [12] was prevented. Special attention was given to the position of the posterior papillary muscle [13] in order to avoid valve distortion. One of our patients did not receive a prosthetic ring (patient 6) and had nevertheless good early result. Unfortunately, reoperation was necessary 0.7 years later for leaflet retraction, but without annulus dilatation.

Intraoperative control echocardiography demonstrated one early stenosis and three patients with a mild MV insufficiency. There was no correlation between excellent early results and/or mild residual MV insufficiency regarding the evolution toward valve deterioration. In this series, a technical factor predisposing to valve failure can be excluded except in the patient presenting residual MV stenosis after implantation.

4.2. Homograft storage
A large debate regarding the durability of cryopreserved versus ‘homovital’ homograft exists. Most results were elaborated from the aortic homograft experience. In cryopreservation without antibiotics, viability of endothelial cells is decreased but still present 3 weeks after harvesting [14]. On mid-term examination, explantation of cryopreserved aortic homografts do not demonstrate cell growth or metabolic function [15], even when collagen appeared to be preserved. In explanted aortic homografts from living donors, the structure of the collagen is perserved early after explantation [15]. Low dose antibiotics (homovital aortic homograft) appear to decrease immunologic stimulation (in vitro) [16].

The storage technique used in our series when the MH was obtained from a multiorgan donor is a combination of the two described techniques. Due to the conditions during multiorgan harvesting it appeared appropriate to use low dose antibiotics for 24 h in order to assure a sterile homograft. No correlation between the two groups (antibiotics and cryopreservation versus cryopreservation alone) regarding the incidence of homograft valve degeneration was observed.

4.3. Immunology
Very little is known with respect to the antigenicity of the MV. Aortic homografts in primates appear to have a decreased antigenicity [17]. One of the main differences between the aortic valve and the MV is the presence of muscle tissue in the subvalvular apparatus of the MV. Muscular tissue results in greater immunologic stimulation and production of antibodies from the recipient [8]. Conditioning of papillary muscles with glutaraldehyde [9] was presumed to decrease immunologic stimulation and the risk of necrosis. However, the rate of papillary muscle dysfunction was not reduced by glutaraldehyde as reported by Kumar et al. [9] and this technique is no longer used.

One of our patients (patient 11) received cyclosporin following homograft insertion. However, immunodepression did not prevent early failure (0.7 years) and this patient was reoperated. Attempts at immunodepression with azothioprine have been used in children undergoing cryopreserved aortic allograft [18]. Allo-immune human leukocyte antigens (HLA) antibody response in such cases was not reduced and the influence on graft dysfunction was not significant. A high incidence of infection was underlined by Hawkins et al. as an important drawback to this protocol [19].

Experimental studies such as cyclosporine in the rat [20] or {gamma} interferon [21] in vitro have been demonstrated to decrease T-cell response to valve allograft. However, immunodepression cannot be extensively used in children.

Blood group mismatch appears to have no effect on the outcome of the homograft as previously published by Schutz et al. [22] and confirmed in our series. Production of antibodies to HLA has not been proven to be a risk of homograft degeneration [23].

In conclusion, due to the early occurrence of degeneration, MV homograft replacement should not be used in young patients.


   Footnotes
 
Presented at the 16th Annual Meeting of the European Association for Cardio-thoracic Surgery, Monte Carlo, Monaco, September 22–25, 2002.


   Appendix A. Conference discussion
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A. Conference...
References
 
Dr V. DiSesa (Philadelphia, Pennsylvania, USA): Do you have a similar experience with aortic homografts in young patients? And do you believe that an immune reaction is a significant component of your observations?

Dr Chauvaud: We have not an extensive experience of aortic valve replacement in children and young patients.

Reviewing all the literature on this subject, there is a lot of confusion about the causes of degeneration. Most probably it's from immunologic origin, but it's not totally clear which kind of process is involved.

Dr C. Yankah (Berlin, Germany): I congratulate you for this very interesting study and results with the critical comments. I do also agree with your conclusion, entirely, that this type of valve replacement is not suitable for children or young patients. My question is more technical. How did you size the valves for the replacement?

Dr Chauvaud: We followed strictly the Acar's guidelines regarding to the size of the annulus of the recipient compared to the size of a homograft and also the length of the anterior leaflet. We adapted the length of the chordae to the distance between the tip of a papillary muscle to the annulus,during the implantation of the homograft.

Dr A. Moritz (Frankfurt, Germany): May I ask you, the difference between the durability of the aortic homograft is not as catastrophic as this mitral homograft, fortunately. But the durability of the pulmonary side seems to be somewhat better than the aortic, so it may very well be that the mechanical stress plays a role. Do you have any experience, or do you know, there are only a few cases I think reported about the tricuspid homograft, is there an improved durability compared to the mitral?

Dr Chauvaud: In our experience, and in what is published on the tricuspid replacement with mitral homograft on the tricuspid valve, patients are adults. And we know that a gradient of 5–10 mm could be well tolerated on the right side. At the present time, I have no data, about early degeneration of mitral homograft on the right side compared to what I presented on the left side.

Dr Acar: I just wish to make a comment in addition to Dr Chauvaud's presentation. Regarding the durability of the mitral homograft, presently we are reviewing the whole series of patients. We have a series of over 90 cases, including two-thirds of complete homograft and one-third of partial homograft. Definitely, as Sylvain just mentioned, it's the durability that doesn't seem to meet the expectation, and we do not feel that we can recommend today using a mitral homograft in a young patient. This could have been a good alternative to bioprosthetic valve since there is no idea of substitute in this age group. But meanwhile, waiting for the complete results of our series, which has now a 10-year follow-up, we feel that it is not a good alternative in this age group.

Dr C. Mestres (Barcelona, Spain): You just mentioned that there is degeneration in both the chordae tendineae. But at which level, tip of the papillary muscle, halfway the chordae in the subleaflet area, or whatever? And you say that 20 h before cryopreservation, that means how was warm ischemic time and cold ischemic time on the average?

Dr Chauvaud: Regarding the final aspect of a chordae tendineae, there is an absence of endothelium and the collagen is totally disorganized, the inflammatory response on the chordae is very weak. Inflammation is much more important on the leaflet tissue itself. The ischemic time was 25 h between harvesting and cryopreservation. Is that the answer you expected?

Dr Mestres: I was asking how long was the warm ischemic time and the cold ischemic time?

Dr Chauvaud: The warm ischemic time is very short. As soon as the heart is arrested, it is placed in cold saline, which is not cryopreservation. And later it is prepared for cryopreservation.


   References
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 

  1. Baskett R.J., Ross D.B., Nanton M.A., Murphy D.A. Factors in the early failure of cryopreserved homograft pulmonary valves in children: preserved immunogenicity?. J Thorac Cardiovasc Surg 1996;112:1170-1179.[Abstract/Free Full Text]
  2. Jones T.K., Lupinetti F.M. Comparison of Ross procedures and aortic valve allografts in children. Ann Thorac Surg 1998;66:S170-S173.
  3. Luciani G.B., Casali G., Santini F., Mazucco A. Aortic root replacement in adolescents and young adults: composite graft versus homograft or autograft. Ann Thorac Surg 1998;66:S189-S193.
  4. Acar C., Tolan M., Berrebi A., Gaer J., Gouezo R., Marchix T., Gerota J., Chauvaud S., Fabiani J.N., Deloche A., Carpentier A. Homograft replacement of the mitral valve graft selection, technique of implantation, and results in forty-three patients. J Thorac Cardiovasc Surg 1996;111:367-380.[Abstract/Free Full Text]
  5. Gross C., Klima U., Mair R., Brücke P. Aortic homografts versus mechanical valves in aortic valve replacement in young patients: a retrospective study. Ann Thorac Surg 1998;66:S194-S197.
  6. Plunkett M.D., Schneider D.J., Shah J.J., Bash S.E., Bond L.M., Geiss D.M. Homograft replacement of mitral valve in children. Ann Thorac Surg 1998;66:849-852.[Abstract/Free Full Text]
  7. Clarke D.R., Campbell D.N., Hayward A.R., Bishop D.A. Degeneration of aortic allografts in young recipients. J Thorac Cardiovasc 1993;105:934-942.[Abstract]
  8. Rajani B., Mee R.B., Ratliff N.B. Evidence for rejection of homograft cardiac valves in infants. J Thorac Cardiovasc Surg 1998;115:111-117.[Abstract/Free Full Text]
  9. Kumar A.S., Choudhary S.K., Mathur A., Saxena A., Roy R., Chopra P. Homograft mitral valve replacement: five years results. J Thorac Cardiovasc Surg 2000;120:450-458.[Abstract/Free Full Text]
  10. Doty D.B., Acar C. Mitral valve replacement with homograft. Ann Thorac Surg 1998;66:2127-2131.[Abstract/Free Full Text]
  11. Chauvaud S., Kalangos A., Berrebi A., Gaer J., Acar C., Carpentier A. Systemic lupus erythematosus valvulitis: mitral valve replacement with a homograft. Ann Thorac Surg 1995;60:1803-1805.[Abstract/Free Full Text]
  12. Yankah A.C., Sievers H.H., Lange P.E., Bernhard A. Clinical report on stentless mitral allografts. J Heart Valve Dis 1995;4:40-44.[Medline]
  13. Cochran R.P., Kunzelman K.S. Effect of papillary muscle position on mitral valve function: relationship to homografts. Ann Thorac Surg 1998;66:S155-S161.
  14. Lang S.J., Girodano M.S., Cardon-Cardo C., Summers B.D., Staiano-Coico L., Hajjar D.P. Biochemical and cellular characterization of cardiac valve tissue after cryopreservation or antibiotic preservation. J Thorac Cardiovasc Surg 1994;108:63-67.[Abstract/Free Full Text]
  15. Mitchell R.N., Jonas R.A., Schoen F.J. Pathology of explanted cryopreserved allograft heart valves: comparison with aortic valves from orthotopic heart transplants. J Thorac Cardiovasc Surg 1998;115:118-127.[Abstract/Free Full Text]
  16. Johnson D.L., Sloan C., O'Halloran A., Yacoub M.H. Effect of antibiotic pretreatment on immunogenicity of human heart valves and component cells. Ann Thorac Surg 1998;66:S221-S224.
  17. Kawauchi M., Nakajima J., Takeda M., Oka T., Takamoto S. Aortic valves are antigenic but less so than myocardium. J Thorac Cardiovasc Surg 1998;116:532.[Free Full Text]
  18. Shaddy R.E., Lambert L.M., Fuller T.C., Profaizer T., Thompson D.D., Baker S.I., Osborne K.A., Hawkins J.A. Prospective randomized trial of azathioprine in cryopreserved valved allografts in children. Ann Thorac Surg 2001;71:43-47.[Abstract/Free Full Text]
  19. Hawkins J.A., Breinholt J.P., Lambert L.M., Fuller T.C., Profaizer T., McGough E.C., Shaddy R.E. Class I and Class II anti-HLA antibodies after implantation of cryopreserved allograft mateiral in pediatric patients. J Thorac Cardiovasc Surg 2000;1198:324-330.
  20. Légaré J.F., Ross D.B., Issekutz T.B., Ruigrok W., Creaser K., Hirsch G.M., Lee T. Prevention of allograft heart valve failure in a rat model. J Thorac Cardiovasc Surg 2001;122:310-317.[Abstract/Free Full Text]
  21. Batten P., McCormack A.M., Rose M.L., Yacoub M.H. J Thorac Cardiovasc Surg 2001;122:129-135.[Abstract/Free Full Text]
  22. Schutz A., Fischlein T., Breuer M., Haushofer M., Uhlig A., Detter C., Kemkes B.M., Hammer C., Reuchart B. Cytoimmunological monitoring after homograft valve replacement. Eur J Cardiothorac Surg 1994;8(11):609-612.[Abstract]
  23. Smith J.D., Hornick P.I., Rasmi N., Rose M.L., Yacoub M.H. Effect of HLA mismatching and antibody status on "homovital" aortic valve homograft performance. Ann Thorac Surg 1998;66:S212-S215.



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