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J Thorac Cardiovasc Surg 1994;107:424-0437
© 1994 Mosby, Inc.
Surgery for Acquired Heart Disease |
From the Department of Cardiovascular Surgery, University of Padova School of Medicine, Padova, Italy; the National Heart Hospital, London, England; the Department of Cardiovascular Surgery, Linz General Hospital, Linz, Austria; the Department of Cardiovascular Surgery, Jagiellonian University, Krakow, Poland; the Department of Mechanical Engineering, University of Surrey, Surrey, England; the Oxford Homograft Bank, Oxford, England; and the Department of Anatomy, University of Verona School of Medicine, Verona, Italy.
Address for reprints: Gino Gerosa, MD, Istituto di Chirurgia Cardiovascolare, Università degli Studi, Via Giustiniani, 2, 35128 Padova—Italy.
Abstract
The increasing use of the aortic homograft as aortic valve substitute and the limited availability of donor valves prompted us to consider the pulmonary homograft as an alternative substitute for aortic valve replacement. The aim of our study is to compare the ultrastructural and biomechanical properties of pulmonary homograft leaflets with those of their aortic counterpart and to present the early results of using the pulmonary homograft for aortic valve replacement. Light and transmission electron microscopy have shown that pulmonary homograft leaflets are thinner than the aortic with a lesser content of elastic tissue in the ventricularis layer. However there were no substantial differences in the ultrastructure. Uniaxial tensile tests were done on 69 cusps from human pulmonary and aortic valves using an Instron testing machine. The strain at 200 KPa was found to be similar for both pulmonary and aortic leaflets (8.20% ± 2.87% versus 8.98% ± 1.90%) cut circumferentially. Radial strips appear to be more extensible in pulmonary leaflets than in aortic (32.6% ± 7.5% and 28.6% ± 11.1%, respectively). The ultimate tensile strength for circumferential strips was found to be similar for both aortic and pulmonary valves (1460 ± 857 kPa versus 1450 ± 689 kPa), but there was relatively little difference between the radial strips (295 ± 95 kPa versus 252 ± 104 kPa). A total of 123 patients whose ages ranged between 13 and 78 years received either fresh antibiotic sterilized or cryopreserved pulmonary homografts for aortic valve replacement. The pulmonary homograft was inserted in place of the patient's diseased aortic valve by using one of two different techniques: freehand in the subcoronary position or as a "short cylinder" inside the aortic root. There were three hospital deaths (2.43%; 70% confidence limits = 1.08% to 4.83%). Cumulative follow-up was 184 patient-years (range 1 to 39 months). All surviving patients have been followed up with serial color flow Doppler echocardiography. There were no late deaths. Actuarial late survival was 97.5% (70% confidence limits = 95.7% to 98.6%) at 3 years. Four patients (2.2%/pt-yr) underwent reoperation because of severe aortic regurgitation (1, 4, 12, and 15 months after the operation) because of technical problems (mismatch in size between the pulmonary homograft and aortic anulus) in three patients and probably because of graft rejection in one patient. At 3 years the actuarial rate of freedom from reoperation was 95.5% (70% confidence limits = 92.7% to 97.3%). Mild aortic regurgitation has been detected in three patients (2.6%). No patients incurred thromboembolic episodes or infective endocarditis. According to our results the pulmonary homograft has ultrastructural and biomechanical properties similar to those of the aortic homograft. Furthermore, the pulmonary homograft is more pliable and easier to insert, giving promising short-term results. (J THORAC CARDIOVASC SURG 1994;107:424-37)
In 1962 Ross
1 first introduced the use of aortic homografts for aortic valve replacement. Since then several studies have shown satisfactory long-term results when either fresh or cryopreserved aortic valves were used. Durability far exceeded porcine xenografts when cryopreserved homografts were used. 2-4
This procedure is an established method, but its wide use is restricted by the limited availability of homograft valves. To overcome this restriction we considered the pulmonary homograft to be a suitable alternative.
The pulmonary valve usually can be harvested even when its aortic counterpart has to be discarded because of atherosclerotic or calcific lesions. In the clinical setting, pulmonary homografts function well when used for right ventricular outflow tract reconstruction 5 and the autogenous pulmonary valve demonstrates excellent long-term results when transplanted in the aortic position. 6 Furthermore, preliminary studies have recently reported promising short-term results by using the pulmonary homograft for aortic valve replacement, therefore allowing a greater number of patients to receive homograft valves. 7, 8
The present study was undertaken to investigate the ultrastructure and tensile properties of human pulmonary valve leaflets and to compare them with their aortic counterparts. In addition we reviewed the clinical data concerning 123 patients who underwent aortic valve replacement with a pulmonary homograft at two different institutions: Department of Cardiovascular Surgery of Linz General Hospital (Austria) and Department of Cardiovascular Surgery, University of Krakow (Poland).
LIGHT AND ELECTRON MICROSCOPY STUDY
Material and methods
Five human hearts with normal valves by gross inspection were harvested from cadavers within 48 hours of death during routine autopsies. The donor ages ranged between 65 and 73 years (mean 68 ± 7 years). Both the aortic and pulmonary valves from each heart were dissected. None of the valves was frozen before the study.
For transmission electron microscopy the valves were fixed in 2.5% glutaraldehyde in Sorensen buffer for 2 hours, postfixed in 1% osmium tetroxide in the same buffer for 1 hour, dehydrated in graded ethanols, embedded in Epon araldite, and cut with a Reichert Ultracut E ultramicrotome (Erich Reichart, Freden, Germany). Semithin sections were stained with toluidine blue and observed by light microscopy. Ultrathin sections were stained with lead citrate and uranyl acetate and observed under a Zeiss EM10 electron microscope (Carl Zeiss, Inc., Thornwood, N.Y.).
As a control all fragments were also processed for scanning electron microscopy.
Results
By light microscopy, the aortic and pulmonary valves showed a similar structure even though the aortic valve was slightly thicker. By transmission electron microscopy, some differences were found between the aortic and the pulmonary valves, in the composition of the lamina fibrosa and the lamina ventricularis. The aortic valve had a thicker lamina ventricularis with elastic fibers of a larger size than the pulmonary valve (Fig. 1, A and B).
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In pulmonary valves, the lamina fibrosa was thinner than in the aortic valves and the collagen fibers were less closely packed. Among the collagen fibers, numerous small elastic fibers were visible and the "cement substance" usually was more scarce than in aortic valves (Fig. 1, D). Both the pulmonary and aortic valves exhibited a spongiosa of similar structure, although that of the aortic valve was thicker than that of the pulmonary valve.
UNIAXIAL TENSILE TESTS
Material and methods
Of the mechanical testing methods described in the literature, uniaxial tensile testing is the simplest for providing data from which a basic comparison of valves can be drawn. The test regimen was based on that of Lee, Courtmann, and Boughner, 9 which was considered to be the most comprehensively described.
Eleven pairs of fresh human aortic and pulmonary valves (i.e., from 11 hearts) and one extra pulmonary valve, all stored in antibiotic medium, were received from the Oxford Heart Valve Bank, John Radcliffe Hospital, Oxford, England. These valves had been rejected as not suitable for use as replacement valves but were undamaged in the regions of interest for uniaxial tests. The donor ages ranged between 19 and 90 years (mean 49 ± 19 years).
The sample preparation was always performed by the same experimenter to minimize handling and measurement errors. Parallel blades, 10 mm apart for radial samples and 5 mm apart for circumferential samples, were used to cut 69 leaflets. The leaflets were always cut in the manner shown in Fig. 2, avoiding inclusion of the lunules or nodule in the test specimen. The third leaflet of each valve was alternately cut radially or circumferentially, but in the same direction for valves from the same heart
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9 Gauge length was measured at zero load, after cycling, by measuring the distance between the clamp jaws with vernier calipers. The samples were then tested to failure at the same extension rate. Load and displacement were continuously monitored from transducers on the Instron 4501 test machine by a data logger (Fig. 3). Failure was considered to be the point at which a dramatic drop in load occurred.
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9 were derived.
Statistical analysis
Statistical analyses for each parameter (ultimate tensile strength, posttransitional modulus, and strain at 200 kPa) were performed with paired t tests for samples from the same heart and unpaired t tests when all the data were used (significance was noted at p = 0.05 for both types of test). The results are tabulated ± one standard deviation.
Results
The results (summarized in Table I and Fig. 4) show first that there is a fourfold difference in mechanical properties in the circumferential versus the radial direction within a valve and second that our population of aortic and pulmonary valves exhibit similar values when a given direction is being compared (e.g., radial, Table I, B). Within a heart, there is a significant difference in strain at 200 kPa between the aortic and pulmonary valves (Table I, C).
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CLINICAL EXPERIENCE
Patients and methods
One hundred twenty-three patients underwent replacement of the aortic valve with a pulmonary homograft at Linz Hospital (Austria) from September 1988 to January 1992 (N = 61) and at Krakow Hospital (Poland) from February 1989 to December 1991 (N = 62). There were 80 male (65%) and 43 female (35%) patients with an age range from 13 to 78 years (mean ± standard deviation 51.9 ± 18.2 years). Indications for operation were aortic stenosis in 52 patients (42.3%), aortic regurgitation in 23 (18.7%), a mixed aortic valve disease in 46 (37.4%), aortic prosthetic endocarditis in 1 (0.8%), and aortic prosthesis dysfunction in 1 (0.8%). At the time of operation 94 patients (76.4%) were in New York Heart Association functional class III and 23 (18.7%) in class IV. Concomitant operative procedures were performed in 26 patients (21%) as listed in Table II.
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The criteria of Edmunds and coworkers 10 were used to categorize valve-related complications. Aortic regurgitation was assessed by Doppler study in accordance with criteria of Perry and coworkers. 11
Statistical analysis
Event-free actuarial analysis for death, valve-related death, valve removal, first valve-related event, and first event was conducted by the product-limit method of Kaplan and Meier. 12 Homogeneity of event-free rates was tested by the log-rank statistic where appropriate. Significant differences in event-free rates were searched for in the presence of nonoverlapping 70% confidence limits (CL) around each event. Cumulative incidence of event (cumulative hazard function) was calculated as the negative logarithm of the freedom from event estimate. Linearized rates of occurrence were calculated as the number of events divided by the total follow-up accumulated after hospital discharge and expressed as percent per patient-year at risk. 13 Crude rates and actuarial probability estimates are presented with associated 70% confidence limits. Where applicable, continuous variables are presented as ± one standard deviation.
All statistical analyses were conducted at University of Liverpool (Clinical Data) and University of Surrey (Mechanical Testing) (by M.J. and S.M.). A p value less than 0.05 was considered significant.
Surgical techniques and homograft procurement
All operations were performed with the patient supported by cardiopulmonary bypass under moderate hypothermia with cold potassium cardioplegia associated with topical cooling for myocardial protection. Two different techniques were used by the surgeons (P.B. and A.D.) at the two institutions for insertion of the pulmonary homograft.
Technique 1
The Linz group inserted the homograft freehand in the subcoronary position using a modified technique described by Barratt-Boyes and colleagues. 4 The proximal anastomosis was performed with a continuous suture with six threads of 4-0 coated polyester fiber (Ethibond, Ethicon, Inc., Somerville, N.J.) and the distal anastomosis was done by the same technique with only two threads of 4-0 Ethibond suture. The noncoronary sinus was not scalloped to maintain the distance between the commissures (Fig. 5).
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Technique 2
The Krakow group inserted the homograft as a "short cylinder" with a lower suture line of multiple interrupted simple stitches of 4-0 Mersilene suture (Ethicon) and a continuous upper line of 4-0 Prolene suture (Ethicon). Two holes were cut out in two sinuses of the pulmonary homograft to expose the two coronary orifices. The wall of the homograft was subsequently sutured side by side to the coronary ostia with a running 5-0 Prolene suture. Additional mattress sutures were then placed in the noncoronary sinus to obliterate any dead space (Fig. 6).
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Results
Three early deaths occurred, for a hospital mortality of 2.43% (70% CL = 1.08% to 4.83%). One patient with severe coronary artery disease died of low cardiac output resulting from myocardial infarction. One death was due to complications of acute renal failure consequent to a transfusion incident. The third patient died of a massive cerebral stroke: this death therefore has to be considered valve related (0.8%; 70% CL = 0.13% to 2.72%). All deaths occurred in the Linz group (4.91%; 70% CL = 2.19% to 9.62%). There were no late deaths and there were no episodes of bacterial endocarditis. Actuarial late survival was 97.5% (70% CL = 95.7% to 98.6%) at 3 years (Fig. 7). No patient received anticoagulation after the operation and no thromboembolic episodes occurred.
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All the explanted homografts were implanted in the Linz group of patients with the freehand technique (described as technique 1, Fig. 5) (6.90%; 70% CL = 1.9% to 16.7%), giving an incidence of 4.4%/pt-yr. In contrast, no homograft inserted as a "short cylinder" has been removed so far. This difference was statistically significant (p = 0.04). The actuarial rate of freedom from reoperation for the whole group of patients was 95.5% (70% CL = 92.7% to 97.3%) at 3 years, whereas the actuarial rate of freedom from reoperation in the Linz group was 91% (70% CL = 85.6% to 94.6%) (Figs. 8 and 9).
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The use of the aortic homograft as an aortic valve substitute is eliciting widespread interest. Unfortunately, despite the increasing number of valve banks processing homografts, routine aortic valve replacement with aortic homografts is restricted by the limited availability of donor valves. Additionally, a shortage of aortic homografts with a diameter larger than 23 mm makes patients with a dilated aortic anulus unsuitable for this procedure. 7 These practical reasons are leading today's surgeons to investigate the pulmonary homograft as a feasible alternative. Despite the fact that pulmonary autografts have been used since 1967 6 and thefirst study 14 reporting on the use of pulmonary homografts to replace aortic valves was reported in 1970, few reports 15, 16 focusing on the ultrastructural and mechanical characteristics of the pulmonary valve are available.
The pulmonary artery wall has less calcium and elastic tissue than the aortic wall, with probably a lower tendency to intrinsic calcification when used for right ventricular outflow tract reconstruction. 17 In our comparative study we did not find striking differences in ultrastructure between the aortic and pulmonary leaflets. The lamina fibrosa, which plays a major role in the mechanical properties of the leaflets, is thinner in the pulmonary valve than in the aortic valve, and the "cement substance" is more scarce in the pulmonary leaflets. This "cement substance," composed of proteoglycans, has a double task—to link the collagenous fibrils and to provide interfibrillar lubrication. Whether these differences may affect biomechanical specificity of pulmonary leaflets needs to be established.
Differences in the ultrastructure of the pulmonary valve leaflets could also be "age related." Nevertheless, the number of valves included in our study was insufficient to investigate this aspect and to determine the relationship between age and remodeling of the leaflet. The in vitro comparison performed in our study was done with a pair of aortic and pulmonary valves harvested from the same hearts. For this reason the warm ischemic time that elapsed between death and harvesting and fixation of the specimens should not impair the results.
Pulmonary cusps during fetal development bear systemic level pressure. This level of pressure modifies the structure and should enable the pulmonary valve to withstand diastolic aortic pressure when implanted in the left side of the heart. Nevertheless, the ability of the pulmonary valve to tolerate systemic pressure soon after implantation in the aortic position is a major concern.
Uniaxial tensile tests in our study proved that the pulmonary leaflets have mean strain, ultimate tensile strength, and elastic modulus similar to those of their aortic counterparts. Moreover, as previously described for the aortic valve, 18 the pulmonary cusps exhibit important quantitative differences in stress-strain properties in circumferential and radial directions. These findings associated to the similar behavior in extensibility would suggest that the collagen fibers retain the same geometric organization in both the aortic and pulmonary leaflets.
According to our results, there is a difference in the "extensibility" of the pulmonary and the aortic valves harvested from the same heart, but 
Table I, B indicates that the spread in the population hides this difference. Thus extensibility has some bearing on the autograft procedure but none on the allograft procedure. Nevertheless, because of the greater extensibility the pulmonary leaflets should retain a greater resilience enhancing the resistance to fatigue. This extensibility should allow the pulmonary valve to close completely, rendering it competent even when systemic pressure is applied backward. 16 As a matter of fact, the results of mechanical testing herein presented are strongly supported by the results of similar uniaxial tensile tests performed on porcine pulmonary and aortic valves, either fresh or glutaraldehyde treated. 19 In a more recent study, we have shown that failure stress was not affected for either the pulmonary or aortic porcine valves after the valve was cycled in a fatigue test system (personal data).
The thinner pulmonary cusps have a lower cross-sectional area and therefore should fail at a lower load. In vivo, this should have no influence because the in vitro loads exceed the stress that a valve would experience under physiologic conditions.
In our series there were three hospital deaths. One, caused by a cerebral stroke 10 days after the operation, was considered valve related. However, the patient was older than 60 years of age, and in the elderly population stroke is not an uncommon risk. All the surviving patients have been discharged from the hospital without any anticoagulant regimen and no late episodes of thromboembolism have occurred.
Four valves have been removed in the early phase: the pulmonary homograft (cryopreserved) explanted after 4 months showed findings similar to that of graft rejection. Unfortunately we cannot provide further data concerning the presence of viable donor cells in the explanted homograft. Indeed, the occurrence of early homograft failure may be related to the presence of high cellular viability when homovital or highly viable valves are used. 20, 21
In the remaining three cases, the pulmonary homografts were removed because of progressive worsening of existing regurgitation with progression of clinical symptoms. As already mentioned, all the valves removed came from the Linz series. Two reasons have been suggested to explain this failure: a cusp prolapse resulting from imperfect alignment of the commissures or a mismatch in size between the pulmonary homograft and the aortic anulus leading to inadequate leaflet coaptation area.
A previous report from the Stanford group, 22 focusing on correct sizing of homografts by means of intraoperative echocardiography, can support this fact. In their experience one patient who had aortic valve replacement with a pulmonary homograft required rereplacement because of progressive aortic regurgitation over the following 10 months. In this patient the chosen pulmonary homograft at the time of implantation was approximately 4 mm smaller than the diameter of the aortic anulus. Furthermore, Lupinetti and colleagues 7 validated this concept with their findings.
To overcome this problem, the Linz group began to implant homograft valves with an internal diameter 1 to 2 mm larger than that of the aortic ring. Since then no further cases of valve failure resulting from geometric pitfalls have occurred.
Consistent with this result is the fact that this strategy was carried out by the Krakow group from the beginning of their experience and no valves have been removed in their series. The accurate size measurement of the aortic orifice after meticulous total excision of the calcified aortic valve is essential to avoid implantation of a too large homograft, which may cause systolic thrill and rapid leaflet degeneration. On the other hand, implantation of too small a graft may result in early regurgitation.
The larger diameter of the pulmonary valve should improve the already excellent hemodynamic characteristics of homograft valves. The mean pressure gradient measured in a small series of patients receiving a pulmonary homograft for aortic valve replacement was 5.6 ± 3.3 mm Hg, which was significantly lower than the gradient measured in a comparable series of patients receiving an aortic homograft (mean gradient 9.8 ± 5.1 mm Hg) (p < 0.01) (Peter Brucke, personal communication, 1992).
Concern has been expressed about the potential progression of mild aortic regurgitation detected postoperatively in three patients. Current clinical experiences with patients who received a pulmonary autograft 23 or underwent anatomic correction of transposition of the great arteries 24 did not demonstrate progression of pulmonary valve incompetence during long-term follow-up. Nevertheless, we should emphasize that those valves, at the time of implantation, are autogenous and fully viable, thus probably providing an active remodeling.
In conclusion, according to our results, the pulmonary homograft appears to be a suitable alternative for aortic valve replacement as a result of ultrastructural and biomechanical properties. The greater availability, the larger diameter, and the thinner pliable wall are additional advantages when compared with the aortic homograft. Nevertheless, a longer follow-up is required to confirm these satisfactory clinical short-term results, and a rigorous and cautious evaluation is still mandatory.
Appendix: DISCUSSION
Dr. Charles Yankah (Berlin, Germany).
Because the base of the pulmonary allograft is part of the right ventricular outflow tract (infundibular tract), the skirt diameter is wider than the pulmonary valve ring. With the Barratt-Boyes technique, the valve ring diameter must be reduced by at least 2 mm. Doing so might cause some discrepancy in the size. The Ross technique might allow more room to implant an allograft size almost equal to the size of the patient's measured anulus. This avoids an overstretching of the commissures when the commissures are being fixed. If a smaller valve size is used, the inclination may be to overstretch the commissure, and that might affect the long-term results leading to progressive valve insufficiency. I would like to draw attention to this technical point.
Placement of the infundibular skirt below the anulus is bound to result in some compression and folding of the valve, and that may cause stenosis as well as early degeneration.
Which type of technique did you use in your different combined series—the Ross technique or the Barratt-Boyes technique? Which patients had postoperative valve incompetence and gradients during your long-term or midterm follow-up?
Sir Brian Barratt-Boyes (Auckland, New Zealand).
Despite these very good short-term results, I am extremely concerned about this valve as a substitute in the aortic position. We must be careful not to transfer the good results with the pulmonary autograft to the pulmonary homograft. The autograft is a viable valve that remains viable, does not reject, and adapts to the aortic position, just as it does in the transposition arterial switch procedure. The homograft valve that you are using is different and will not adapt. Moreover, it undergoes structural change from the host reaction. None of your tensile tests would indicate that the pulmonary allograft is really comparable to the aortic allograft.
We can think of it very simply by comparing it to the sail on a yacht. If you put up a thin sail on a yacht, the only way that sail will not tear, as opposed to a thicker sail, is if you alter the material of which the thin sail is composed to make it stronger. The simple fact is that pulmonary valve is much thinner than the aortic valve, has a much smaller collagen content, and will therefore fail sooner than the thicker aortic leaflet. This is a simple engineering principle.
I was unwise enough 30 years ago to insert wrapped unstented pulmonary allografts in the mitral position, and of course that is even worse than in the aortic position. They all failed within a few years because of cusp tears. Thus I would predict that this is not a suitable device, and I would suggest that we wait for your longer-term results to see if the pulmonary allograft is a suitable alternative to the aortic allograft.
Dr. Gerosa.
I would like to thank both the discussants for their proposed questions. In response to Dr. Yankah, the Linz group inserted the pulmonary homograft freehand in the subcoronary position using a modified technique described by Barratt-Boyes, performing the proximal anastomosis with a continuous suture using six threads of 4-0 coated polyester fiber and using only two threads of Ethibond 4-0 suture for the distal anastomosis. The Krakow group implanted the homograft with the "short cylinder" technique using multiple interrupted simple stitches for the lower suture line. Valve incompetence during the follow-up was detected only in patients included in the Linz group. In addition, the Linz group studied intraoperatively the hemodynamic performances of both pulmonary and aortic homografts implanted freehand in the subcoronary position. They realized that the gradient across the pulmonary homograft was lower than the gradient across the aortic homograft: the difference was statistically significant. The lower gradient may be related to the fact that the pulmonary homograft has a larger diameter: in fact, we would like to highlight the importance of using a pulmonary homograft at least 1 to 2 mm larger than the recipient's aortic anulus diameter. The oversizing has been shown to reduce geometric pitfalls.
I appreciate the words of warning of Sir Brian Barratt-Boyes concerning the long-term fate of pulmonary homograft inserted in the aortic position. Nevertheless, it is not possible to compare the results of stented pulmonary homografts in the mitral position with unstented pulmonary homografts in the aortic position. Various studies have already demonstrated that the aortic homograft also performs better when implanted freehand in the aortic side rather than when used stented in the mitral position.
To evaluate the mechanical behavior of pulmonary and aortic leaflets, we also tested porcine pulmonary and aortic valves harvested from the same hearts. Those valves were placed in a fatigue test system and were cycled for 484.5 million cycles— an equivalent of 12.75 years in the clinical setting. The uniaxile tensile test performed on those leaflets (this study was done in cooperation with Dr. Boughner of the University of Western Ontario, Canada) have again proved that the pulmonary valve can behave in a manner similar to that of the aortic valve.
Acknowledgments
We are grateful to Mrs. Lara Salviato for preparation of the manuscript, to Mrs. Anna Rambaldo for the illustrations, and to Mark Jackson, PhD, for assistance with the statistical analysis.
Footnotes
Read at the Seventy-second Annual Meeting of The American Association for Thoracic Surgery, Los Angeles, Calif., April 26-29, 1992. 
J THORAC CARDIOVASC SURG 1994;107;424-37.
References
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 F. Della Rocca, S. Sartore, D. Guidolin, B. Bertiplaglia, G. Gerosa, D. Casarotto, and P. Pauletto Cell composition of the human pulmonary valve: a comparative study with the aortic valve-the VESALIO* project Ann. Thorac. Surg., November 1, 2000; 70(5): 1594 - 1600. [Abstract] [Full Text] [PDF]
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