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J Thorac Cardiovasc Surg 1995;110:186-194
© 1995 Mosby, Inc.
SURGERY FOR ACQUIRED HEART DISEASE |
Middlesex and London, England
From Harefield Hospital, Middlesex, and the Royal Brompton and National Heart Hospital, London, England.
Address for reprints: Magdi Yacoub, FRCS, Harefield Hospital, Harefield, Middlesex, UB9 6JH England.
Abstract
Two hundred seventy-five unprocessed, viable homograft ("homovital") aortic valves were used for aortic valve replacement in patients aged 1.5 to 79 years (mean 45.8±19 years) with maximum follow-up of a 14-year period (mean 4.8 years). Ninety-two percent (252 patients) had New York Heart Association class III or IV functional status before operation and 25 underwent emergency operation. Valves were harvested under sterile conditions and kept in nutrient medium 199. Freehand (subcoronary) technique was used in 147 patients and freestanding root replacement was used in 128. Cumulative survival rates for the whole group were 92%±2% at 5 years and 85%±3% at 10 years, as compared with 96%±2% and 94%±4%, respectively, for the 98 patients who underwent isolated root replacement. Multivariate analysis determined that root replacement with associated procedures and operation for prosthetic endocarditis were risk factors for death, whereas previous xenograft valve, operation for endocarditis, and operation for aortic regurgitation were risk factors for reoperation. Actuarial rates for freedom from degenerative valve failure diagnosed at operation, by postmortem examination, or by routine echocardiography were 94%±2% at 5 years and 89%±3% at 10 years. Recipient age younger than 30 years and previous xenograft valve were risk factors for late degeneration. We conclude that homovital valves demonstrate good durability, particularly in patients older than 30 years, who had a 10-year freedom from degeneration rate of 97%. (J THORACCARDIOVASCSURG1995;110:186-94)
To date there is no ideal aortic valve substitute. Homograft aortic valves offer many theoretic and proven advantages, which include restoration of normal flow in the aortic root, sinuses, and coronary orifices; lack of thromboembolism; and resistance to infection.
1-3 These valves also have several disadvantages, however, which include a slightly more complex technique of insertion, limited availability, and limited durability. The last factor is the most important because it necessitates reoperation, with attendant risk, inconvenience, and cost. Two of the most important determinants of durability are the methods of sterilization and methods of preservation of the homograft. Earlier methods, which include chemical (B propriolactone) preservation, irradiation, 4, 5 and freeze drying, 6 have been shown to have a profound deleterious effect on the long-term performance of the homograft valve. In more recent years, antibiotic sterilization 7-9 and cryopreservation 10-12 have resulted in significant improvements in long-term performance of homograft valves. These improvements have been attributed to preserved "viability" of the component cells of the homograft. 10 We and others have shown that cells in the homograft cusp express major histocompatibility antigens both in human beings 13 and in experimental animals 14; however, "viability" could alter the immunologic behavior of the valve. This concern has prompted the suggestion that immunosuppressive agents, with all their potentially serious side effects, could be indicated in patients receiving a viable valve. 15 All forms of valve processing, including antibiotic sterilization and cryopreservation, have the potential to alter the viability as well as the physical and antigenic properties of the valve. To establish the effects of each form of sterilization on long-term functionality of the aortic homograft, it is essential to determine the behavior of the unprocessed, fully viable homograft. The purpose of this article is to analyze our experience with aortic homografts—harvested under sterile conditions from cardiac transplant recipients or brain dead multiorgan donors, kept in tissue-culture medium, and inserted at the first available opportunity—to determine their long-term performance and attempt to define determinants of patient survival likelihood and valve function.
PATIENTS AND METHODS
Between February 1980 and October 1993, 275 patients underwent aortic valve replacement with unprocessed, viable homograft ("homovital") aortic valves. Their ages ranged from 1.5 to 79 years (mean 45.8 ± 19 years). Twenty-two (8%) were aged 16 years or younger. There were 188 (68.4%) male and 87 (31.6%) female patients. The indication for operation was aortic stenosis in 96 patients, aortic regurgitation in 123 patients, and mixed lesions in 56 patients. Twenty-three patients had New York Heart Association (NYHA) functional class II status, 162 had class III status, and 90 had class IV status. The operation was performed electively in 250 cases and as an emergency procedure in 25 cases. Pertinent patient data, as well as variables relating to the homograft valve and the operation, are given in the Appendix.
Homograft data
The homograft valves were harvested under sterile conditions from cardiac transplant recipients in 224 cases and from brain-dead multiorgan donors in 51 cases. The donors varied in age from 10 to 66 years (mean 42 ± 13 years). The original disease of the cardiac transplant recipients was ischemic heart disease in 93 cases, cardiomyopathy in 101 cases, congenital heart disease in 14 cases, and other diseases in 16 cases. The valves were immediately placed in 199 tissue culture medium containing extremely small doses of penicillin and kept at 4º C until used at the first opportunity. The interval of time between harvesting and insertion varied from 2 hours to 60 days (mean 3.9 ± 7 days), with the vast majority inserted within 3 days of harvest (Fig. 1). All donors were seronegative for human immunodeficiency virus and hepatitis B surface antigen.
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4 with a lower interrupted and upper continuous suture line in 147 patients (53.5%). This technique was used if the available valve matched the size of the patient's aortic root, with a diameter equal to or (ideally) 1 to 2 mm smaller than that of the patient's aortic root. The remaining 128 patients underwent replacement of the aortic root with implantation of the coronary arteries. 16 This technique was used when there was a mismatch in size or shape between the homograft and the patient's aortic root and in patients with aortic root disease. 17
Follow-up and data analysis
At the end of the study in March 1994, there were nine early (
30 days after operation) and 16 late deaths. Of the remaining 250 patients, 13 could not be traced. The status of 34 was determined by means of mailed questionnaires and telephone contact, whereas the remaining 203 patients were seen at our hospital during the period of July 1993 through March 1994. The follow-up investigation included physical examination, electrocardiography, and chest radiography. In addition, echo Doppler studies, including color-flow mapping, were performed in 197 patients. Aortic regurgitation was classified as absent or in one of four grades: trivial, mild, moderate, and severe. Presumed degenerative valve failure was defined as moderate or severe valve malfunction discovered at reoperation or post mortem examination, as well as moderate or severe regurgitation or stenosis (with a gradient of 
50 mm Hg) diagnosed by routine echo Doppler imaging in the absence of previous or current endocarditis.
Statistical analysis
BMDP computer programs 18 were used for the statistical analyses. Simple comparisons between groups were done by use of a one-way analysis of a nonpaired t test variance or a standard (Pearson) 
2 test as appropriate. Linear relations were checked by a standard least-squares correlation analysis. The Kaplan-Meier product-limit method was used in the estimation of long-term survival and event-freedom (freedom from valve related complications) probability curves; differences between curves were checked by the log-rank (Mantel-Cox) and the generalized Wilcoxon (Gehan) tests. Long-term survival and event-freedom estimates are given plus or minus one standard error of the mean (SEM). Multivariate analysis of long-term survival and freedom from valve-related complication rates was performed with the proportional hazard regression model introduced by Cox. 19 We adhered strictly to a comprehensive, formalized analysis sequence as described elsewhere. 20 The formalized analysis sequence was developed to make the regression models as reproducible as possible. Variables considered in the tests are given in the Appendix. The level of significance was set at 0.05.
RESULTS
Survival
Among all patients, the cumulative survival rates were 95% ± 1% at 1 year, 92% ± 2% at 5 years, and 85% ± 3% at 10 years (Fig. 2). Patients who underwent isolated aortic root replacement had survival rates of 96% ± 2% at 5 years and 94% ± 4% at 10 years (Fig. 3). These rates were slightly but not significantly better than those in patients who underwent isolated aortic valve replacement by means of the freehand two-suture line technique, who had survival rates of 93% ± 3% at 5 years and 88% ± 5% at 10 years. In contrast, patients who underwent associated procedures in combination with root replacement or subcoronary insertion of aortic homografts had significantly (p = 0.05) lower long-term survival rates, 86% ± 4% at 5 years and 77% ± 7% at 10 years (Fig. 3). Similarly, patients older than 70 years had a 5-year survival rate of 71% ± 12%, compared with 93% ± 2% for those younger than that age (p = 0.004). Multivariate analysis of possible determinants of long-term survival identified operation for prosthetic endocarditis (p = 0.01) and root replacement with associated procedures (p = 0.03) as risk factors. The observed 10-year survival rate among patients free of any of these risk factors (n = 187) was 91% ± 3%.
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Table I).
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Table II); 190 patients without either risk factor had a 10-year freedom from valve degeneration rate of 97% ± 2%.
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Table III).
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Table IV). The rate for 10-year freedom from valve-related complications for 180 patients with none of these risk factors was 94% ± 3%.
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This study shows that the use of homovital (unprocessed) homografts to replace the aortic valve or root gives good early and medium-term results, which compare favorably with those for the use of "processed" valves. It also shows, however, that the use of fully viable valves does not eliminate the risk of slow, late degeneration, and several risk factors for late degeneration or death were found. The pattern of survival rates after homovital homograft replacement reflects the low operative risk, particularly for patients undergoing isolated valve or root replacement, who had a 30-day mortality rate of 0.6%, as well as the low late mortality for the whole group. This low risk was particularly apparent for patients of any age undergoing isolated root replacement, who had a 10-year survival rate, including in-hospital deaths, of 94% ± 4%. The good long-term survival rate could be related in part to the nearly normal flow pattern in the root of the aorta, which may help maintain coronary flow and ventricular function, as well as to the low valve failure rate during the period of follow-up. In this series, the only criterion for inclusion was the availability of a homovital valve; no patient was excluded because of advanced age or poor clinical condition. This selection pattern is reflected by the fact that 25 patients were operated on on an emergency basis and 90 patients had NYHA class IV functional status. Long-term survival rate appeared to be adversely affected by the need for additional procedures, age 70 years or older, and poor left ventricular function before operation.
One of the most important determinants of the results of valve replacement with tissue valves is durability. Durability can be affected by the quality of the tissue, the method of preparation and insertion, and any reaction from the host's immune system. Before insertion, unprocessed tissue homografts have ideal design, physical characteristics, and biologic characteristics. Processes aimed at maintaining sterility and allowing storage can alter the biologic, physical, and antigenic properties of the valve. 21-28 The aortic valve and wall express major histocompatability antigens as well as adhesion molecules; this indicates their capacity to stimulate and be a target for humoral as well as cell-mediated immune response. 13, 14, 26 However, the exact effects of any possible immunologic damage on long-term function of the homograft have not been determined in clinical series. On theoretic grounds, the fact that the aortic valve is avascular and the suggestion that the aortic root is immunologically "privileged" could have important roles in slowing down or halting immune-mediated damage. Furthermore, recent series that used relatively viable valves 8-12 showed improved results. These results support the notion that immune damage may play a minor role. Our study is the first relatively large study to evaluate the performance of a truly viable, unprocessed homograft. In this series, most (98%) but not all of the valves were used within 3 days and therefore can be regarded as "homovital" from the biologic standpoint. The rate of degeneration in these valves has been slow, with no evidence of accelerated failure caused by rejection. We used a rigorous set of criteria to define presumed degenerative valve failure; these criteria were designed to include all patients with significant, nonendocarditis-induced valve dysfunction discovered during routine echocardiographic examination, at reoperation, or after death. The rates of freedom from this complication in the whole series were 94% ± 2% at 5 years and 89% ± 2% at 10 years, which compare favorably with those in other series that used processed homografts. 4, 5, 8-12 This correspondence indicates that true viability is an advantage. The use of these valves, however, has resulted in a definite but slow rate of degeneration, 0.89% per patient-year during the first 7 years accelerating to 2.58% per patient-year during the second 7-year period. These data indicate that "homovital" valves are subject to rejection or are affected by other biochemical or hemodynamic factors. The rate of degeneration in the longer term and its determinants need to be studied further. Matching for ABO blood group did not appear to influence the rate of degeneration during the period of follow-up, and the role of HLA matching could not be determined because of the small number of samples that have been processed at this point; this factor is the subject of a longer term study. The higher incidence of late degeneration among younger recipients, as well as after the use of valves from younger donors, could be caused by differences in the immune systems of children 29 and the increased cellularity of homografts from younger donors. 30 Despite the faster rate of degeneration of homografts in children than in adults, homografts inserted in children function for longer periods than do xenografts 31 and do not appear to adversely affect long-term survival because of their slow mode of failure and the low risk of reoperation. We therefore believe that, at least for the time being, homovital homografts should be considered as an alternative to pulmonary valve autografts 32, 15 in this age group. Aortic root replacement allows the insertion of adult-sized homografts in even small children. 17 Reoperation after aortic root replacement can be achieved with low morbidity and mortality rates. 33 We are currently evaluating the use of homografts versus autografts in this age group in a prospective randomized trial.
In this series, previous xenograft replacement of the aortic valve appeared to increase the rate of late degeneration of the homovital valve. This finding is difficult to explain and needs to be validated or challenged in the future. It is possible, however, that previous xenograft valves can alter the immunologic behavior of the host or the hemodynamic performance of the homograft as a result of distortion of the aortic root. Homovital valves appear to give excellent results in patients older than 30 years who did not have a previous xenograft valve, with a rate for freedom from presumed degenerative valve failure of 97% ± 2%. 10 years after operation.
By means of the Cox regression model, in an attempt to evaluate the expected performance of homovital valves for patients with different characteristics, we estimated the probabilities for a 15-year-old boy who had undergone, previous valvotomy for congenital aortic stenosis, had NYHA class II functional status as a result of severe aortic regurgitation, and underwent isolated root replacement with a valve from a donor aged 25 years. The estimated 10-year survival probability was 93%, and the probability of freedom from presumed degenerative valve failure at 10 years was 73% if root replacement was used and 63% if the two-suture line technique was used (Fig. 5). In contrast, the estimated 10-year survival probability for a 70-year-old man who had severe aortic stenosis, had NYHA class III functional status, and underwent isolated root replacement with a valve from a 50-year-old donor was 87%, with a probability of freedom from presumed degeneration at 10 years of 97% (Fig. 5). The 10-year rate for freedom from endocarditis observed in our study (94%) is identical to that previously reported after the use of antibiotic-sterilized or cryopreserved homografts. 10, 12
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Eighty percent of the valves used in this series were obtained from cardiac transplant recipients. These patients were studied extensively before operation with regard to both valve function and presence or absence of bacterial or viral infection. Although a significant number (n = 101) underwent transplantation for cardiomyopathy, which is known to be associated with persistance of a coxsackievirus genome in the myocardium in a number of patients, 34 this virus is altered, and because it has lost its capacity to replicate it is not infective. This conclusion is supported by our clinical observations. Transplant recipients therefore represent an important additional source of homograft valves. 35
This study has shown that the interval between harvesting and insertion does not appear to affect outcome. This could be because most of the valves were inserted within 48 hours and the period of follow-up and the number of events were not sufficiently large to show such an effect. This is an on-going study to determine the effects of these factors as well as of others, including HLA matching, on outcome. We hope that the data presented in this article are useful in guiding clinical practice, as well as evolving new strategies for improving long-term performance of the grafts in the high-risk groups for failure without increasing the risk to patients.
Appendix: DISCUSSION
Dr. Antonio F. Corno (Milan, Italy).
I have two questions, Mr. Yacoub. First, did you observe fast degeneration in the pediatric population, associated with the need for early homograft replacement? Second, do you suggest any low age limit for the use of this type of "homovital" homograft?
Mr. Yacoub.
These are very relevant questions. We believe that although the rate of degeneration in children is faster than in adults, it is still acceptable and is so much better than that for xenografts. In addition, we have shown that reoperation with the use of another homograft carries a low risk and is followed by excellent long-term survival. Therefore multiple valve replacements could enable the child to reach adulthood, at which point the rate of degeneration is lower. Whether this policy produces similar or superior results to pulmonary autograft replacement at the beginning needs to be investigated further.
Dr. Jan M. Quaegebeur (New York, N.Y.).
Mr. Yacoub, you have shown that the homovital grafts were usually used within the first 3 days after they were collected. However, a certain number of grafts were implanted only later, some of them 2 months after harvesting. Undoubtedly, these grafts must have lost a degree of viability. Have you analyzed the influence of time between harvesting and implantation on valve function and later degeneration?
Mr. Yacoub.
In reply to the second question, there is no detectable influence of the interval between harvesting and insertion on either survival or valve degeneration. However, the number of valves inserted beyond 3 days after harvesting was too small to allow meaningful conclusions to be made.
Dr. Tirone E. David (Toronto, Ontario, Canada).
Sir Madgi, I was very impressed with the actuarial survival. This is likely the best valve to keep the patients alive, but at some point the valve begins to fail. Isn't this failure caused by calcification of the arterial wall of the homograft? Don't you think that the leaflets begin to degenerate when the donor root or the remnants of the arterial wall calcify and increase the mechanical stress on the leaflets?
Mr. Yacoub.
In our own experience the rate of degeneration after root replacement in the adult population is extremely low and appears to be slightly slower than that for the two-sutureline technique. The aortic wall of the root shows minimal or no calcification after homovital root replacement and certainly does not appear to influence valve function. The opposite is probably true.
Dr. David.
Why does the graft fail earlier in younger patients? I thought younger patients had a more active immune system and the valve would calcify more readily.
Mr. Yacoub.
With regard to the cause of the faster rate of degeneration in children, it is possible that the immune system of the younger patient is more active. Alternatively, these patients tend to receive valves from younger donors. Such valves are more cellular and possibly more immunogeneic. In addition, biochemically, the younger patients, as we know from the xenograft experience, tend to have a different way of reacting to foreign tissue. These issues need to be investigated further.
Mr. Ali Rahman (Manchester, England).
Sir Magdi, you have suggested an immunologic reaction of a weak nature, an immunologic reaction especially when xenografts have been used in the past in the same patient. Would you consider using a mild form of immunosuppression in some of these patients to avoid rejection and consequent valve dysfunction?
Mr. Yacoub.
With regard to the finding of faster degeneration of homografts in patients who had previous xenograft replacement, it is possible that local or immunologic factors could be operative. We believe that this finding needs to be confirmed or refuted in future studies. The other point relates to immunosuppression. We believe that the currently available immunosuppressive agents have many serious side effects that would be much more important than the slow rate of degeneration of the valve even in the high-risk groups. In contrast, manipulations of the homograft tissue before insertion with a view to altering the immune response to such tissue might be a possibility for the future.
Dr. Endre Bodnar (Pinner, Middlesex, United Kingdom).
I have two questions. First, do you have any evidence that these valves, which are called homovital and you imply would be viable, are truly viable? Second, you attributed the failure of these valves to an immunologic reaction. Have you seen any evidence of rejection--macroscopic, microscopic, or histochemical—in those valves that you have removed?
Mr. Yacoub.
With regard to the question of viability, these valves were dissected within minutes of procurement from the donor at the time of transplantation and kept in tissue culture medium until inserted, generally within 3 days. Solid organs like kidneys treated in a similar fashion are known to be fully viable. As for the evidence for immunologic reaction, this needs further studies. We have data showing that after homovital homograft replacement, anti-HLA antibodies are formed, which appear to be donor-specific. However, the possible effect of such reaction on long-term performance has yet to be investigated.
Dr. Bodnar.
My reason for asking these questions was that your statements and conclusion contradict the entire current concept of preserving homografts. If valves are stored in a nutrient solution for more than 48 hours, many people, such as Marc O'Brien and others, would say that those valves are no longer viable. They have laboratory evidence, not a personal belief, but scientifically sound laboratory evidence, to prove that viability is definitely lost after 7 days.
Mr. Yacoub.
In the current study we speculated that an immune response is involved by exclusion. In this series, the valves were obtained under sterile conditions and were not subjected to high concentrations of antibiotics at any time. They were used within 3 days in almost all cases and therefore were truly viable.
Appendix: APPENDIX
Preoperative patient-related, homograft-related, and intraoperative data considered in the multivariate analyses (number of patients or mean ± standard deviation)
Patient-related data.
Male (n = 188) or female (n = 87) sex; age (46 ± 19 years); NYHA functional class II (n = 23), III (n = 162), or IV (n = 90); left ventricular end-diastolic dimension (58 ± 13 mm) and fractional shortening (33% ± 12%) at echocardiography; previous aortic valve procedure, none (n = 189), homograft (n = 32), or autograft (n = 2) aortic valve replacement, valvotomy or repair/resuspension (n = 29), and xenograft (n = 14) or mechanical valve (n = 9) aortic valve replacement; dominant aortic valve or prosthetic valve lesion, stenosis (n = 96), regurgitation (n = 122), and mixed lesion (n = 57); native (n = 11) or prosthetic valve (n = 7) endocarditis; original congenital (n = 25), bicuspid (n = 77), rheumatic (n = 33), calcific (n = 54), infectious (n = 23), and other or undetermined (n = 54) etiology or Marfan syndrome (n = 9).
Homograft-related data.
Donor age (42 ± 13 years); male (n = 221) or female (n = 54) donor sex; any combination of donor-recipient sex; donor diagnosis, cardiomyopathy (n = 101), ischemic heart disease (n = 93), congenital heart disease (n = 14), emphysema and cor pulmonale (n = 13), cystic fibrosis and cor pulmonale (n = 3), brain-dead multiorgan donor (n = 51); donor-recipient ABO compatible (n = 129), incompatible (n = 100), "feasible" (n = 46; O to A, B or AB); time from harvest to implantation (3.9 ± 6.6 days).
Intraoperative data.
Operative procedure, subcoronary aortic valve replacement isolated (n = 88) or with associated operation (n = 59), root replacement isolated (n = 89) or with associated operation (n = 39); associated operation, none (n = 189), mitral valve replacement (n = 6) or repair (n = 10), coronary artery bypass (n = 45), tailoring of ascending aorta (n = 20), repair of congenital malformation (n = 12) or combinations (n = 5); elective (n = 250) or emergency (n = 25) operation.
Footnotes
Read at the Seventy-fourth Annual Meeting of The American Association for Thoracic Surgery, New York, N.Y., April 24-27, 1994. 
References
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J.-M. Grinda, C. Latremouille, N. D'Attellis, A. Berrebi, S. Chauvaud, A. Carpentier, J.-N. Fabiani, and A |
