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Ann Thorac Surg 1999;67:1617-1622
© 1999 The Society of Thoracic Surgeons

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Original Articles

Cryopreserved aortic allografts for aortic root reconstruction: a single institution’s experience

^a Department of Cardiothoracic Surgery, St. Antonius Hospital, Nieuwegein, the Netherlands
^b Department of Cardiology, St. Antonius Hospital, Nieuwegein, the Netherlands

Accepted for publication December 12, 1998.

Address reprint requests to Dr Dossche, Dept of Cardiothoracic Surgery, St. Antonius Hospital, Koekoekslaan 1, 3435 CM Nieuwegein, the Netherlands

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. An evaluation of early and long-term results of aortic root replacement with cryopreserved aortic allografts and echocardiographic follow-up of allograft valve function was performed.

Methods. From September 1989 through May 1998, 132 patients aged 17 to 77 years (mean, 50.8 ± 14.8 years) underwent freestanding aortic root replacement with a cryopreserved aortic allograft. Eighty-six (65.1%) patients had New York Heart Association class III or IV functional status before operation, and 27 (20.5%) patients underwent emergency operation. Fifty-nine (44.7%) patients had undergone previous cardiac operations. The cause of aortic disease was acute endocarditis in 63 (47.7%) patients, healed endocarditis in 15 (11.3%), degenerative in 20 (15.2%), congenital in 20 (15.2%), failed prosthesis in 10 (7.6%) and rheumatic in 4 (3.0%). Follow-up was complete, with a mean of 42 months.

Results. There were 12 hospital deaths (9.1%; 70% confidence limits [CL], 6.6% and 11.6%); 9 of them were operated on for active endocarditis (p = 0.062). Multivariate analysis determined age older than 65 years (p = 0.012) and emergency operation (p = 0.009) as independent risk factors for hospital mortality. During follow-up, 6 (5.0%; 70% CL, 3.0% and 7.0%) patients died. Cumulative survival rate for the entire group was 81.8% ± 5.4% at 8 years. Freedom from reoperation for structural valve failure was 100%, freedom from reoperation for any cause was 96.3% ± 1.8% at 8 years. Freedom from endocarditis at 8 years was 97.9% ± 1.4%. Follow-up of allograft valve function showed no or trivial aortic regurgitation in 97% of patients and absence of stenosis of the allograft in 100%.

Conclusions. Aortic root replacement with cryopreserved aortic allografts can be performed with acceptable hospital mortality and long-term results. The durability of cryopreserved aortic allografts is good, and reoperation for structural valve failure is absent at 8 years.

	Introduction

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Allograft aortic valve implantations have been performed clinically for the past two decades with increasing demand. Methods of sterilization and storage are known to have a profound influence on the long-term performance of allograft valves. Irradiated and chemically sterilized valves were shown to have an unacceptable propensity for cusp rupture [1, 2]. In more recent years, fresh antibiotic-sterilized aortic allografts have been used, but they have the disadvantage of a finite storage time of approximately 1 month [3–6]. O’Brien and colleagues [7] developed the techniques currently used for allograft valve cryopreservation, making them readily available for use by many surgeons. Both techniques have resulted in significant improvements in long-term performance of the allograft valves, because of the preserved viability of the component cells of the allograft [8].

The purpose of this article is to analyze our experience with cryopreserved aortic allografts used for freestanding aortic root replacement (ARR), including a long-term clinical and echocardiographic functional evaluation.

	Material and methods

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From September 1989 through May 1998, 132 patients underwent ARR with a cryopreserved aortic allograft. Their ages ranged from 17 to 77 years (mean, 50.8 ± 14.8 years). There were 99 (75.0%) male and 33 (25.0%) female patients. The indication for operation was aortic stenosis in 15 patients, aortic regurgitation in 104, and mixed lesions in 13. Eighty-six (65.1%) patients had New York Heart Association (NYHA) functional class III or IV. The operation was performed electively in 105 (79.5%) patients and as an emergency procedure in 27 (20.5%) patients. Left ventricular ejection fraction was at least 50% in 119 (90.0%) of patients. Other pertinent patient data, as well as variables relating to the operation are given in the Appendix.

Allograft data
Aortic allograft valves were harvested under sterile conditions from cardiac transplant recipients, beating-heart or non–beating-heart donors, age 18 to 65 years. Dissection of the heart was generally performed within 24 hours after circulatory arrest. After dissection, the valves were decontaminated by incubation in medium with an antibiotic mixture for 5 hours at 37°C. Thereafter, valves were cryopreserved in medium containing 10% dimethylsulfoxide (DMSO) frozen at a controlled rate of -1°C/min up to -100°C and stored on the vapor of liquid nitrogen (-150° to -196°C). All tissues were cryopreserved within 50 hours after circulatory arrest of the donor. All donors were seronegative for human immunodeficiency virus, hepatitis B surface and core antigen, cytomegalovirus or Treponema pallidum. For implantation, ABO compatibility was not required. In elective operations, mismatch in age between the donor valve and recipient was avoided; in emergency operations this was possible only occasionally. All allografts were provided by Bio Implant Services Foundation (BIS), Leiden, the Netherlands.

Operative technique
Standard cardiopulmonary bypass was used. Cold crystalloid antegrade cardioplegia was administrated selectively through the coronary ostia with intermittent cardioplegic reinfusion. During cardioplegic arrest, the myocardial septal temperature was kept at 10°C. All diseased aorta or aortic valve was excised, retaining good-sized buttons of aorta around the coronary arteries. After removal of redundant septal myocardium and the anterior mitral leaflet, the allograft was attached to the outflow tract in a horizontal, subannular plane. A continuous suture technique using three 4-0 polypropylene sutures was used in 92 (69.7%) patients; interrupted 4-0 polypropylene sutures were used in 40 (30.3%) patients. In 78 (59.1%) patients, hemostasis and support was improved by means of a Teflon felt—although not in patients with active native or prosthetic valve endocarditis—or pericardial ring incorporated into the suture line. The allograft coronary arteries were excised, and the recipient coronary arteries were anastomosed directly with continuous 6-0 polypropylene suture. The distal end of the allograft was then attached in an end-to-end fashion to the recipient ascending aorta with continuous 5-0 polypropylene suture.

Fifty-nine (44.7%) patients had prior cardiac operations, 58 of them for aortic valve disease and 1 for coronary artery bypass grafting. Twenty-four (18.2%) patients had a concomitant procedure at the time of the ARR. A cryopreserved allograft with an internal diameter less than 23 mm was implanted in 18 (13.7%) patients, internal diameter 23 to 25 mm in 96 (72.6%) patients, and greater than 25 mm in 18 (13.7%) patients. If the diameter of the recipient aortic annulus exceeded 27 mm or the Z + 2 value for the calculated body surface area, a reduction annuloplasty was performed (n = 5) [9]. Aortic cross-clamp time ranged from 68 to 257 minutes (mean, 117 ± 32 minutes). Extracorporeal circulation time ranged from 92 to 364 minutes (mean, 166 ± 54 minutes). Aprotinin, tranexamic acid, or other hemostatic agents were not routinely used.

Follow-up
The status of all hospital survivors was determined by recent (< 6 months) information from the patient’s cardiologist or by visit at our cardiology department. Closing date for follow-up was June 30, 1998. Follow-up included physical examination, electrocardiography, and chest radiography. Valve function was assessed either clinically by auscultation or by echo Doppler study including color-flow mapping. Aortic diastolic murmurs were graded on a scale of 0 to 4, with 0 representing no audible murmur and 4 representing a severe murmur. At echocardiography, allograft regurgitation was graded on a scale of 0 to 4. A valve with no incompetence was graded as 0, trivial incompetence as 1, mild incompetence as 2, moderate incompetence as 3, and severe incompetence as 4. Valve stenosis was graded as present (gradient 30 mm Hg) or absent.

Data analysis
Data from all consecutive patients who underwent allograft ARR were reviewed retrospectively. Quantitative data are presented as mean ± standard deviation. Univariate comparisons between groups were calculated by the unpaired test, Fisher’s exact test, ² test, or the one-way or two-way analysis of variance as appropriate. All probabilities are two-tailed. Kaplan-Meier survival curves were used for analysis of survival times, and Tarone or Breslow test for comparisons between survival curves. Odds ratios for factors associated with hospital death (see Appendix) were obtained using multivariate logistic regression models. Precision was indicated by 70% confidence limits (CL).

	Results

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Mortality
Overall hospital mortality was 9.1% (n = 12; 70% CL, 6.6% and 11.6%). For patients having a root replacement for active native or prosthetic valve endocarditis, mortality was 14.3% (9 of 63; 70% CL, 9.9% and 18.7%); for other conditions, mortality was 4.3% (3 of 69; 70% CL; 2.9% and 6.7%) (p = 0.063). Mortality for reoperations was 8.5% (5 of 59; 70% CL, 4.9% and 12.1%) versus 9.5% (7 of 73; 70% CL, 6.1% and 12.9%) for primary operations (p = 0.824). In case of concomitant procedures, mortality was 12.5% (3 of 24; 70% CL, 5.8% and 19.2%) versus 8.3% (9 of 108; 70% CL, 5.7% and 10.9%) for simple ARR (p = 0.536). Six deaths resulted from sepsis or multiorgan failure, 2 patients died of low cardiac output, another 2 died of severe central neurologic damage after resuscitation on the ward. One patient died of a technical failure at the beginning of our experience, and another patient in whom the allograft adventitia was removed during processing died of rupture of the aortic allograft wall (proven by autopsy) on the 30th postoperative day. Variables entered in a stepwise logistic regression to identify risk factors for hospital mortality were age, preoperative NYHA functional class, previous cardiac operation, active endocarditis, concomitant procedures, emergency operation, and pump time. Multivariate analysis identified age older than 65 years (p = 0.012) and emergency operation (p = 0.009) as incremental risk factors for hospital mortality; the probability of dying in the hospital was 2.3% in the absence (p = 0.000) of any incremental risk factors, but was increased significantly if the patient was older than 65 years (5.9 times) or in cases of emergency operation (9.9 times) (Table 1).

Late outcome
Mean length of follow-up for all patients was 42 months (range, 2 to 102 months); total follow-up for the series was 393 patient-years. No patients were lost to follow-up. During follow-up, 6 of the 120 hospital survivors died (5%; 70% CL, 3.0% and 7.0%). Three of these deaths were noncardiac related. One patient died after reoperation for early endocarditis of the allograft valve, resulting in a false aneurysm at the proximal suture line. Two patients died suddenly, 1 month and 5 years after operation, without any known cause. The hazard function had a rapidly falling early phase of risk during the first month after operation and a low constant hazard extending during the entire period of follow-up. Actuarial survival (including hospital deaths) for the overall group at 1, 5, and 8 years was 89.8% ± 2.7%, 85.7% ± 4.1%, and 81.8% ± 5.4%, respectively. The difference in survival between patients with acute endocarditis (71.0% ± 11.8%) and those free from active endocarditis (88.9% ± 5.7%) at time of the operation was not significant (p = 0.089) (Fig 1).

View larger version (25K): [in this window] [in a new window]   Fig 1. Estimated survival after allograft aortic root replacement, including hospital mortality (n = 132). (NVE = native valve endocarditis; PVE = prosthetic valve endocarditis.)

View larger version (24K): [in this window] [in a new window]   Fig 2. Freedom from endocarditis after allograft aortic root replacement, excluding hospital deaths (n = 120). (NVE = native valve endocarditis; PVE = prosthetic valve endocarditis.)

Allograft valve function
An echocardiographic assessment of the allograft valve function was done routinely within 6 weeks after operation. Data of 125 patients (before discharge or within 6 weeks after operation) are listed in Table 3. During follow-up, allograft regurgitation was assessed either clinically (diastolic murmur) or by transthoracic echocardiography with color flow. Of the 120 hospital survivors, 98 patients had a follow-up longer than 1 year. In 3 of them, no diastolic murmur was heard at physical examination. Echocardiographic data of 95 other patients are listed in Table 3.

	Comment

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From the beginning of our allograft experience in 1989, the freestanding root replacement technique has been our technique of choice for two reasons. First, in this technique, the allograft is used as a geometrically single functional unit. As such, the intercommissural distance is appropriate and fixed, and the sinotubular dimensions are therefore less susceptible to distortion during the suspension of the commissural posts. This is expected to reduce both early and late postoperative regurgitation [10, 11]. Second, nearly half of the treated patients in our series had active endocarditis and as such complex aortic root disease. In these situations, as well as in situations of unusual valvular anatomy, the anatomy of the allograft root offers additional advantages. The soft annulus with its muscular cuff can fill subannular defects and help restore atrioventricular continuity. We and others have reported good early and late results with this surgical approach [12–15].

The overall hospital mortality of 9.1% in our series for ARR is significantly higher than what is generally acceptable for aortic valve replacement. This is not related to the technical aspects of the procedure but to the complexity of the patients included in the series. Nine of the 12 deaths were patients with active endocarditis and all had extensive aortic root disease including aortic root abscesses. In only 1 patient, at the beginning of our experience, did a fatal technical failure occur. Therefore, we do not think that the root replacement technique places the surgical patient at any added immediate operative risk. Prager and associates [16] reported similar results in their series of 71 patients undergoing allograft ARR. Hospital mortality was 17% and occurred mainly in situations of complex root disease such as aortic dissection or extensive root infection [16]. Recent publications on the use of cryopreserved allografts report a hospital mortality between 1% and 3%, although most of the implantations were done in an infracoronary position. Only by occasion was an ARR performed, which was associated with a considerably higher mortality rate [17, 18]. O’Brien and colleagues [10], who routinely perform root replacement in all their allograft procedures, reported a hospital mortality rate of 1.7%. No significant difference in hospital mortality between the infracoronary and root replacement technique was reported by Yacoub and associates [6]. In experienced hands, the root replacement technique can be done with low hospital mortality.

Structural valve degeneration remains a central issue in assessing the long-term durability of the cryopreserved aortic allograft. McGiffin [19] depicted the interrelationship between overlapping mechanisms of allograft valve failure influenced by known risk factors, eg, younger recipient age, older donor age, larger aortic root diameter, insertion technique, and valve preservation technique. In all patients we have tried to exclude these risk factors as much as possible. Older allografts were not used in younger patients, large aortic roots were reduced to avoid the use of large size allografts, and all allografts were implanted as one functional unit. To date, with a mean follow-up of 42 months, we had no explanations for structural valve degeneration. As the durability test for allograft valves occurs between 10 and 14 years, we cannot yet determine the possible added long-term advantage to our patients of using all allografts for ARR. Overall survival and freedom from all valve-related complications was not different from results observed with (unprocessed) homovital allografts [6]. We could not confirm the additional advantage of these truly viable allografts over the cryopreserved allografts with fewer viable cells.

Recent echocardiographic studies have shown a lower incidence of aortic regurgitation after root replacement than after infracoronary implantation of human tissue valves. Daicoff and coworkers [20] noted progression of aortic insufficiency determined by color-flow Doppler echocardiography in a group of infracoronary allograft implantations, using a fully scalloped allograft. Early after implantation, no patient had aortic regurgitation greater than grade 2/4. During follow-up, 80% of patients had grade 2 or greater regurgitation, and in 40% of these patients, severity was grade 3/4 or 4/4. Jones and associates [21] had a similar experience with infracoronary implanted allografts, retaining the noncoronary sinus, although findings were less extreme compared to the series of Daicoff and colleagues [20]. From our series, there was no obvious progression of the degree of incompetence between the initial echocardiographic data and data obtained during follow-up. This parallels findings of O’Brien and associates [10]. Concerns remain about the potential for late degeneration and calcification of the allograft wall, possible coronary ostial complications, and the risk of reoperation, particularly in the presence of significant calcification. Long-term experience remains small thus far. Sundt and associates [22] reported their experience with reoperations on the aortic root in 22 patients who underwent previous aortic allograft (21 patients) or pulmonary autograft (1 patient) root replacement. Although they initially used either fresh or antibiotic-sterilized and homovital allografts, their findings may be of relevance to the use of cryopreserved allografts as well. Significant calcification of the allograft was present in 52% of patients; however, the coronary ostia were free of calcification. Calcification was, even when severe, limited to the allograft wall itself and was noninvasive. In 41% of patients, a repeat freestanding root replacement was required, whereas in others it was possible to insert a mechanical prosthesis or an infracoronary allograft valve within the previous root. Hospital mortality for these reoperative procedures was 4.5% [22].

In conclusion, replacement of the diseased aortic valve with a cryopreserved allograft offers distinct advantages to the patient over alternative valve substitutes. The root replacement technique respects the sinotubular geometry of the allograft root, which results in a reduced incidence of postoperative regurgitation and may thus result in an improvement of long-term results.

	Appendix

 
Preoperative patient-related and intraoperative data considered in the univariate and multivariate analysis of hospital mortality (number of patients or mean ± standard deviation) are presented.

Patient-related data
Male (n = 99) or female (n = 33) sex; age (50.8 ± 14.8 years); NYHA functional class II (n = 46), III (n = 53), or IV (n = 33); left ventricular ejection fraction at left ventriculography or echocardiography at least 50% (n = 119), between 30% and 50% (n = 12), less than 30% (n = 1); previous aortic valve procedure, none (n = 75), mechanical valve (n = 30), xenograft (n = 19), valvotomy (n = 8), allograft (n = 1); dominant aortic or prosthetic valve lesion, regurgitation (n = 104), stenosis (n = 15), and mixed lesion (n = 13); active native (n = 31) or prosthetic valve endocarditis (n = 32), healed native (n = 10) or prosthetic valve endocarditis (n = 5); complex root abscesses (n = 40), no active annular abscesses (n = 92); preoperative creatinine less than 180 µmol/L (n = 123), at least 180 µmol/L (n = 7), or on hemodialysis (n = 2); valve at present operation tricuspid (n = 63), bicuspid (n = 20), prosthetic valve (n = 49).

Intraoperative data
Operative procedure, root replacement isolated (n = 108) or with associated procedure (n = 24); associated operation, none (n = 108), mitral valve replacement or repair (n = 11), coronary artery bypass grafting (n = 6), closure of ventricular septal defect (n = 6), tricuspid valve plasty (n = 1); continuous (n = 92) or interrupted (n = 40) suture technique; extracorporeal circulation time, less than or equal to 180 minutes (n = 91) or more than 180 minutes (n = 41); aortic cross-clamp time, less than or equal to 120 minutes (n = 79) or more than 120 minutes (n = 53); diameter of implanted aortic allograft, less than 23 mm (n = 20), between 23 and 25 mm (n = 93), more than 25 mm (n = 19); elective (n = 105) or emergency (n = 27) operation.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Marc A.A.M. Schepens Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Dossche, K. M. Articles by Ernst, S. M. Search for Related Content PubMed PubMed Citation Articles by Dossche, K. M. Articles by Ernst, S. M.