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Ann Thorac Surg 2007;84:1564-1570. doi:10.1016/j.athoracsur.2007.02.100
© 2007 The Society of Thoracic Surgeons
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Original Articles: Cardiovascular

Subcoronary Allograft Aortic Valve Replacement: Parametric Risk-Hazard Outcome Analysis to a Minimum of 20 Years

Edward Hickey, MRCSa,b,*, Stephen M. Langley, FRCSa, Oliver Allemby-Smith, MRCSa, Steven A. Livesey, FRCSa, James L. Monro, FRCSa

a Wessex Cardiothoracic Centre, Southampton, United Kingdom
b The Hospital for Sick Children, Toronto, Ontario, Canada

Accepted for publication February 20, 2007.

* Address correspondence to Dr Hickey, The Congenital Heart Surgeons’ Society, The Hospital for Sick Children, Room 4431, 555 University Ave, Toronto, Ontario, M6R 1T3, Canada (Email: edward.hickey{at}sickkids.ca).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Differences in sterilization, preservation, and implantation have been implicated in aortic allograft longevity. We report follow-up to 30 years of patients from a single unit who underwent aortic valve replacement with aortic allografts sterilized in antibiotics and refrigerated at 4°C.

Methods: Two hundred consecutive patients underwent subcoronary allograft aortic valve replacement and have been followed up to a minimum of 20 and maximum of 30 years. Follow-up was 96% complete. Parametric hazard phase modeling was used to identify incremental predictors of time-related risk.

Results: Early mortality was 1.5%. Kaplan–Meier actuarial survival, including early death, was 81.2% ± 2.8% (mean ± standard error of the mean), 58.0% ± 3.7%, and 52% ± 5.1% at 10, 20, and 25 years, respectively. Freedom from reoperation for any reason was 86.4% ± 2.6%, 39.6% ± 5.2%, and 35.0% ± 5.4% at 10, 20, and 25 years, respectively. Larger implanted valve, reexploration for bleeding, previous cardiac surgery, and operative rank were independent risks for reoperation. Early mortality in reoperations was 5.1%. Allograft endocarditis has occurred in 6 patients, giving an overall freedom of 94% at 25 years. Seven patients of the original cohort are known to be alive with their original allograft valve in situ, and of these the longest follow-up period is 29.8 years.

Conclusions: The use of antibiotic-sterilized allografts for subcoronary aortic valve replacement confers low operative mortality and excellent long-term survival with durability matching any other nonmechanical device. Significantly reduced time-related risk of reoperation and excellent internal to external diameter ratio renders allograft aortic valve replacement especially ideal for smaller roots.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Subcoronary allograft aortic valves were first implanted in 1962 [1] and provided an attractive alternative to mechanical prostheses in avoiding the need for systemic anticoagulation. Initially, fresh allografts were used, but their unpredictable availability mandated that methods of sterilization and preservation be developed. Early methods included chemical sterilization with formaldehyde [2], ß-propiolactone [3], and ethylene oxide [4], or sterilization through irradiation and preservation by freeze-drying or storage in a carbon dioxide freezer at –70°C [3]. However, these techniques were associated with unacceptable rates of failure [5, 6], and their use was therefore abandoned in the late 1960s.

Antibiotic sterilization and preservation in nutrient mediums was introduced in 1968 [7], and the technique was associated with long-term durability comparable to that of fresh allografts [8]. Preservation was initially carried out at 4°C, allowing storage for 6 to 8 weeks; however, for many units, the concept of cryopreservation [9]—storage in liquid nitrogen at –168°C—was more attractive, as it allowed for much longer, possibly indefinite, storage. In the early 1970s, therefore, antibiotic storage of allograft valves was largely phased out and cryopreservation has become almost exclusively the method of choice. At our institution, however, early [10] and mid-term [11] results using valves stored in antibiotic medium at 4°C encouraged us to persist in this preservation technique until our local valve bank service was withdrawn in 1991.

Several large series exist describing the long-term outcome with allograft valves [12–14]. However, all of these use a combination of both implantation and preservation techniques, with cryopreservation predominating from the 1970s. This is important, because considerable debate has surrounded the ideal methods of allograft sterilization and preservation.

Because our center used a single allograft processing method and a consistent implantation technique, the series of patients we report represents a unique profile of the long-term function of these valves. Subsequent to previous reports from our unit in which we describe the medium [11] and long-term [15] outcome with these valves, we now conclude our follow-up to a minimum of 20 years and a maximum of 30 years in a series of 200 consecutive patients.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patients
Between January 1973 and December 1983, 200 consecutive patients received subcoronary aortic valve replacement (AVR) with an antibiotic-sterilized allograft at our institution, all of whom were subjected to retrospective analysis. Individual patient consent was not sought because the investigation was historical in nature, but institutional ethical approval was obtained. This series represents 15.5% of the total 1,285 AVR operations performed during this period. At the time, this was a low proportion, explained in part by our use of Carpentier-Edwards and Hancock pig valves for patients older than the age of 70 years from 1976 onward. In addition, after a report by Barratt-Boyes and colleagues in 1977 [8], allograft AVR was avoided when the root diameter exceeded 24 mm, as this was associated with premature failure. Patient demographics and indication for operation are shown in Table 1.


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  		Table 1 Indication for Operation
 
The profile of recipients of allograft valves changed during the course of the study period, largely as a consequence of reduced allograft availability. This was primarily related to the impact of increasing xenograft production from 1976 and the introduction of compulsory consent for donor harvesting in the early 1980s. From this time, allograft valves were therefore most suitably used for women of reproductive age, those with bacterial endocarditis, a bleeding diathesis, or contraindications to anticoagulation, and younger patients. Anticoagulation was not routinely used after isolated allograft AVR, unless an arrhythmia was present. Owing to limited availability, allografts were preferentially used in those younger than 70 years, although elderly women with small roots were considered eligible as allografts have a large internal to external diameter.

Follow-up has taken place through outpatient visits and medical records. The minimum follow-up period was 20 years, and maximum 30 years, providing a total follow-up of 3,164 patient-years. Follow-up was 96% complete.

Valve Preparation
All allografts were procured from donors within 4 days of death (mean, 1.56 ± 0.76 days). Donors were between the ages of 11 and 50 years (mean, 28.2 ± 9.3 years), although the majority were younger than the age of 30 years (65%) and most died of accidents or suicide. In the recognition of the serious risk of transmissible disease associated with tissue transplantation, donors are now screened for hepatitis B surface antigen, human immunodeficiency virus, VDRL test organisms, and hepatitis C virus. Although these measures were introduced only from the late 1980s, we have no knowledge of transmission of infection within our patient population.

The allografts were obtained from routine postmortem examinations. Briefly, the process is as follows: the aortic valve is removed intact, with the anterior mitral valve leaflet retained and flanked by a 5-mm ventricular muscle band, which is subsequently trimmed to 2 mm. A long length of aorta and approximately 5 mm of coronary artery is preserved. After sizing of the valve ring with obturators, the allograft is immersed in antibiotic-nutrient medium at room temperature for 24 hours to allow sterilization. The details of this medium may be important as subtle differences have been implicated in their long-term durability. The valve is then transferred within this medium to an environment refrigerated to 4°C and stored for up to 3 months. Confirmation of sterility is carried out by removing nine sections of 3 mm2 of aortic wall at the time of procurement and treating them in an identical fashion for the first 24 hours. They are then cultured for aerobic, anaerobic, and fungal growth at 4°, 20°, and 37°C for a week. Only after this culture period has confirmed no significant growth are the valves cleared for implantation. Implantation may therefore occur between 9 and 119 days after harvest. All allografts in this series were implanted between 9 and 119 days (mean, 46.7 ± 21.6 days), the majority within 8 weeks (73%; Fig 1).


Figure 1
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  		Fig 1. Profile of duration of valve preservation.

 
Implantation
All operations were performed by one of the two senior surgeons at our institution at the time. Valves were inserted freehand in the subcoronary position with upper and lower continuous suture lines as described by Ross [1] in 72% and Barratt-Boyes [16] in 28%. The dead space between the allograft and host aortic wall was then obliterated with additional mattress sutures. Valve sizes ranged from 15 to 28 mm internal diameter (median, 20 mm; interquartile range,19 to 22 mm), with 165 (82.5%) varying between 18 and 22 mm. The mean duration of cardiopulmonary bypass was 122 ± 30 minutes.

Data Analysis
Data sets were analyzed using SAS statistical software (version 9.1; SAS institute, Inc, Cary, NC). Parametric models of time-related hazard were constructed after hazard decomposition into phases. No significant early-phase or constant-phase components were identified for either death or reoperation, so effectively risk analysis reflects only late-phase remodeling. After bootstrap resampling (n = 1,000), automated stepwise linear regression analysis was undertaken to identify time-related predictors of outcome. Confidence limits are expressed as ± 1 standard deviation (70%) unless otherwise stated, and significance was considered at p less than 0.05.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Early Mortality
There were 3 early (30-day) deaths (1.5%). Two of these were after primary allograft AVR, both for insufficiency. The first was a 56-year-old woman with osteogenesis imperfecta who suffered fatal sudden aortic rupture on the 14th postoperative day. The second was a 55-year-old man who sustained a massive thromboembolic cerebrovascular accident on day 18 and did not recover. The remaining early mortality concerned a 34-year-old man who had active bacterial prosthetic valve endocarditis on a Starr-Edwards aortic valve. It was not possible to wean him from cardiopulmonary bypass, and he died in the operating suite. The early mortality associated with primary aortic valve replacement in our series was therefore 1.1%.

Late Mortality
At the end of the 30-year follow-up period, 81 (40.5%) patients are known to have died. Of the known causes, 41 (59%) were related to cardiac failure or sudden cardiac events. Endocarditis was the cause in 3 (3.7%) and reoperation in 4 (4.9%), reflecting an early mortality at reoperation of 5.1%. Four patients are known to have suffered a fatal cerebrovascular accident (2% of the total cohort, and 4.9% of the late deaths). Kaplan–Meier survival analysis (Fig 2) for any cause of death, including early mortality, reveals 10-, 15-, 20-, and 25-year survival of 80.8% ± 2.8%, 67.8% ± 3.4%, 57.0% ± 3.6%, and 52.0% ± 3.2%, respectively.


Figure 2
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  		Fig 2. Survival after allograft aortic valve replacement. Circles represent the Kaplan–Meier estimate for survival at each death, the solid lines represent the parametric determination of continuous point estimates, and the dashed lines enclose the 70% confidence interval. (A) Percent survival; (B) hazard function.

 
Factors associated with time-related risk of death were identified as emergency operation, a heavily calcified explanted valve, operative procedures in addition to allograft AVR, and the occurrence of a postoperative stroke (Table 2). Notable factors that did not have a significant impact on late death include the need for root tailoring, the use of a gusset, duration of cardiopulmonary bypass or myocardial ischemia, and previous sternotomy or cardiac surgery.


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  		Table 2 Incremental Factors for Increased Time-Related Risk of Death
 
Freedom From Reoperation
Of the original cohort, 78 (39%) patients have undergone reoperation (redo AVR), of whom 4 died (30-day mortality, 5.1%). The mean cardiopulmonary bypass duration during re-replacement was 86 minutes. Calculated and predicted freedom from reoperation (redo) and the associated late-phase hazard function are shown in Figure 3. Kaplan–Meier analysis of freedom from reoperation for any reason is 86.5% ± 2.6%, 70.0% ± 3.8%, 40.3% ± 5.1%, and 36.0% ± 5.4% at 10, 15, 20, and 25 years, respectively. Of the original cohort, excluding those lost to follow-up, 7 (3.5%) patients are known to be alive with their original allograft valve in situ. Of these 7, the longest follow-up period is 29.8 years.


Figure 3
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  		Fig 3. Freedom from reoperation after allograft aortic valve replacement. Circles represent the Kaplan–Meier estimate for freedom at each reoperation event, the solid lines represent the parametric determination of continuous point estimates and the dashed lines enclose the 70% confidence interval. (A) Percent freedom from reoperation; (B) hazard function.

 
Factors associated with time-related risk of reoperation for any cause were identified as a larger size of implanted allograft, the need for reexploration for bleeding, previous sternotomy or cardiac surgery, and operative rank: the risk for reoperation increased with experience (Table 3). The effects of these identified variables on predicted time-related risk of reoperation are shown in Figure 4. Notable factors among those examined that did not have a significant impact on reoperation include the need for root tailoring, the use of a gusset, allograft storage duration, or age of allograft donor.


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  		Table 3 Incremental Factors for Increased Time-Related Risk of Reoperation
 

Figure 4
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  		Fig 4. (A) Risk-adjusted percent freedom from reoperation after allograft aortic valve replacement, stratified by allograft implant size; (B) whether mediastinal reexploration was necessary postoperatively; (C) whether the patient had had previous sternotomy; (D) and the operative rank.

 
Freedom From Endocarditis
Six (3%) patients are known to have suffered allograft valve endocarditis, of whom 3 died as a result. The Kaplan–Meier freedom from allograft valve endocarditis of 94% at 25 years. No perioperative factors were identified that influenced the time-related risk of developing allograft valve endocarditis.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
This report represents a unique insight into the use of allograft aortic valves. It reflects a large patient cohort, all of whom received a subcoronary allograft aortic valve that has been procured, sterilized, preserved, and implanted using a uniform technique and consistent surgical teams. Several reports describe allograft valve [12, 17] and root replacement [18] in large patient series with long follow-up periods. Many of these combine the cohorts of allograft AVR and root replacement, which we believe is inappropriate because the clinical indications, surgical techniques, progression of disease, and indications for reoperation are different for each. The same series typically includes a variety of implantation and preservation techniques. This is important, as during the period of its maximal use considerable controversy surrounded the optimal techniques for the preservation and storage of the allograft valve, with many authors attributing superior longevity to cryopreservation [13]. Currently accepted predictors of poor outcome are instead less subtle: older donor age [12], younger recipient, size-mismatching [19], and full-root versus nonroot replacement [20].

The demise of early chemically treated allograft valves was largely attributed to a lack of cellular viability [5, 21]. The assumption was that donor viability was associated with preserved structural architecture, enhanced elasticity, delayed degeneration, and improved function. Although incubation of antibiotic-sterilized valves at 4°C in nutrient medium [7, 22] may allow allograft tissue to remain viable for a number of days (homovital, viable, or fresh valves), chromosomal studies indicate that longer incubation periods (as in our series) result in little significant residual cellular viability [22]. Flash-freezing does not compromise cellular viability [9] or elasticity [23], and therefore cryopreservation was seen as an answer to dwindling donor populations at a time when bioprosthetic devices were not yet established. The additional proposed benefit was improved cellular viability. Despite encouraging early results [8, 10] with antibiotic-sterilized refrigerated valves, cryopreservation therefore rapidly became the predominant allograft processing method worldwide.

In fact, the link between valve durability and cellular viability is not clear. Much has been made of the demonstration of both donor endothelium and fibroblasts in explanted valves through chromosomal [24] and in situ hybridization studies [25], with the inference that fibroblastic activity enhances architectural integrity [26]. However, other reports instead implicate donor cell viability in the degeneration process [27], perhaps through allograft immunogenicity. Certainly the cryopreservation process can alter the tissue immunogenicity [28], and more recently HLA-DR and ABO donor–recipient mismatch has been shown to influence allograft longevity in pediatric patients [29]. The interesting finding that right-sided grafts appear more prone to cellular rejection than left-sided grafts [30] serves to illustrate that we are only just beginning to uncover the pathologic processes behind allograft degeneration. In fact, decellularization is a necessary prerequisite in the tissue engineering of heart valves. This is attributed at least in part to the retained immunogenicity exhibited by allograft valves with residual cellular viability [31]. In addition, it has been demonstrated that decellularized xenograft valves retain antigenicity in contrast to allograft valves [31].

The outcomes reported here with sterilized, refrigerated valves are extremely favorable, results that we attribute—at least in part—to the processing methods used. The late-phase survival and freedom from reoperation match or exceed almost all significant series of nonmechanical AVR, especially including cryopreserved valves [12], and the favorable freedom from reoperation is especially pertinent given the young age of the allograft recipients. We acknowledge the low incidence of active endocarditis in our population—related in part to the fact that other large series are complicated by the inclusion of allograft root replacements, which we believe are a separate clinicopathologic entity. On the other hand, we have included in our analysis patients with previous sternotomy and having concomitant procedures: comparison of this cohort against modern series reporting primary bioprosthetic AVR is therefore extremely favorable [32–35]. Furthermore, our series describes a young recipient population, and young age has repeatedly been identified as an independent predictor of early failure [12, 17].

The recent popularity of the Ross procedure for aortic valve disease in young adults and children emphasizes the need to revisit the technique of subcoronary valve implantation that we describe in this series. The most frequent technique for autograft valve implantation involves a cylinder root. However, preserving the native sinuses, sinotubular junction, and coronary artery egress seems intuitively attractive, and a recent series examining subcoronary autograft implantation describes midterm outcomes that at least match the cylinder root technique—to the extent that the authors advocate the need for a randomized trial [12–14, 36]. One drawback with the use of subcoronary valve implantation is that it is a more technically demanding and time-consuming procedure to perform. It requires precise matching of the valve size and aortic root, or tailoring to generate a match, and failure to do so has been clearly linked to early failure. Furthermore, the physical properties of the loose and flexible allograft in contrast to modern valve rings mounted on firm holders makes implantation a more lengthy procedure, compounded by the need for two suture lines. Even in experienced hands, the procedure is likely to result in greater durations of cardiopulmonary bypass and myocardial ischemia. This is not, however, reflected in greater early mortality in our or others’ series [36]. We explored the impact of experience by examining the impact of operative rank on late reoperation. Surprisingly, earlier operations had a lower risk of reoperation for reasons we cannot explain, although the parameter estimate is exceptionally small. An elevated mortality risk at reoperation is also commonly cited as a drawback associated with allograft use. In fact, our experience (5.1%) suggests the risk at reoperation to be similar to that for bioprosthetic valve replacement, and this has been confirmed by several other groups [37, 38].

Allograft valves remain a first-line option for the management of endocarditis, a feature necessarily attributed at least in part to their preincubation in antibiotics, as demonstrated in accelerated models of graft infection [39]. The lack of inanimate material also suggests an advantage in terms of acquired endocarditis, a notion supported by the extremely low long-term risk of endocarditis experienced in this series.

This is one of the longest follow-up series describing the use of allograft AVR, and certainly the largest and longest involving a cohort of antibiotic-sterilized valves implanted using a single technique. The extremely favorable early and late mortality, freedom from surgical reintervention, and freedom from endocarditis—especially when compared with modern tissue bioprostheses—confirm their use as an attractive first-line option for the surgical management of aortic valve disease. Remarkably, 7 patients remain well with their original allograft valve in situ at the conclusion of our follow-up to 30 years, confirming antibiotic-sterilized allograft valves to be at least as satisfactory for AVR as any known nonmechanical device. Efforts to increase their availability and enhance training in surgical implantation might offer real patient benefit, and has prompted us to create a homograft bank to increase local availability. Reports of successful large-scale procurement programs, even in countries with alarming levels of transmissible disease, should serve as examples [40]. This series has prompted us to reopen our local allograft valve bank in an effort to increase local availability.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Ross DN. Homograft replacement of the aortic valve Lancet 1962;2:487.[Medline]
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Steven A. Livesey
James L. Monro
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