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Ann Thorac Surg 1998;66:412-416
© 1998 The Society of Thoracic Surgeons


Original articles: cardiovascular

Aortic allograft implantation techniques: pathomorphology and regurgitant jet patterns by doppler echocardiographic studies

Tineke P. Willems, MDa,b, Lex A. Van Herwerden, MD, PhDa, Meindert A. Taams, MD, PhDa, Veronica E. Kleyburg-Linkera,b, Jos R.T.C. Roelandt, MD, PhDa,b, Egbert Bos, MD, PhDa

a Department of Cardio-Pulmonary Surgery, Thoraxcenter, University Hospital Rotterdam-Dijkzigt and Erasmus University, Rotterdam, the Netherlands
b Department of Cardiology, Thoraxcenter, University Hospital Rotterdam-Dijkzigt and Erasmus University, Rotterdam, the Netherlands

Accepted for publication February 26, 1998.

Address reprint requests to Dr van Herwerden, Department of Cardio-Pulmonary Surgery, Bd 156, University Hospital Sophia-Dijkzigt, Dr Molewaterplein 40, 3015 GD Rotterdam, the Netherlands
e-mail: (vanherwerden{at}thch.azr.nl)

Presented at the VII International Symposium on Cardiac Bioprostheses, Sitges, Spain, June 13–15, 1997.


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. The diagnosis of allograft-specific pathology by echocardiography has important consequences for patient counseling and research. This study describes the pathomorphologic findings and color Doppler jet patterns in a consecutive series of patients after allograft placement with either the subcoronary implantation or root replacement technique.

Methods. From 1987 to July 1996, the subcoronary allograft implantation technique and root replacement technique were used in 82 patients and 70 patients, respectively. These patients comprised the study group.

Results. The incidence of paravalvular leaks and eccentric regurgitant jets was higher with subcoronary implantation (41%) than with root replacement (11%). Patients with a subcoronary implanted allograft had a higher incidence of eccentric jets.

Conclusions. These findings support the concept of preservation of valve geometry after root replacement, as allograft-specific pathomorphologic abnormalities and eccentric jets are more common after subcoronary implantation of allografts. Learning effects, however, cannot be excluded as the cause of these abnormalities.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Aortic valve replacement with an allograft is a well-established surgical treatment with good long-term results for cryopreserved [13] and homovital aortic donor valves [4].

Cross-sectional echocardiography and color Doppler echocardiography have been used as noninvasive diagnostic tools to document aortic regurgitation and stenosis after allograft implantation [111]. However, there is a remarkable scarcity of systematic descriptive reports of pathomorphologic echocardiographic findings [5, 12]. These data are important because echocardiography during follow-up is used for the dual purpose of patient counseling and research. In addition, detailed analysis of jet patterns on color Doppler echocardiography could reveal differences between implantation techniques.

The purpose of this study is to describe the pathomorphologic findings and regurgitant jet patterns on two-dimensional and color Doppler echocardiography in a consecutive series of adult patients with cryopreserved allograft aortic valves in whom either the subcoronary implantation technique or the root replacement technique was used.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Patients
Between 1987 and July 1996, 152 adult patients underwent implantation of a cryopreserved allograft aortic valve at the Thoraxcenter, Rotterdam. In 82 patients, the subcoronary implantation technique was used, and in 70 patients, aortic root replacement was performed. The mean age and the sex distribution of the patients were as follows: for subcoronary implantation, 47.9 years (range, 21.8 to 83.6 years) and 70% male, and for aortic root replacement, 47.6 years (range, 17.3 to 75.7 years) and 63% male.

The subcoronary implantation technique was mainly used in patients with aortic valve pathology and intact aortic root. The pathologic process in this group was of rheumatic origin in 13 patients, a bicuspid valve in 25 patients, senile degeneration in 9 patients, and other in 4 patients. Thirty-one patients (38%) had operation for a pathologic condition attributed to infective endocarditis. Eleven of these 31 patients had active endocarditis at the time of implantation, and 5 patients had an annular mycotic aneurysm. Initially, each sinus of Valsalva was excised (32 patients). Subsequently, the allograft valves were implanted with preservation of the aortic wall of the noncoronary sinus (50 patients) [13]. In recent years, the subcoronary implantation technique has been used less frequently.

The aortic root replacement technique was used in 49 patients with aortic valve disease associated with major aortic root pathology, which was caused by acute infective endocarditis in 4 patients. Root replacement was also preferred for 21 patients with aortic valve disease that was not associated with aortic root pathology. The valvular pathologic process in these patients was of rheumatic origin in 2, a bicuspid valve in 5, senile degeneration in 3, and infective endocarditis in 11. Aortic root replacement was performed with a freestanding root and a variable length of donor aorta.

The allograft aortic valves were cryopreserved and supplied mainly by the Heart Valve Bank, Rotterdam, through Bio Implant Services, Leiden, the Netherlands. The mean internal diameter of the allografts was 23.4 mm (range, 19 to 28 mm).

The hospital mortality rate after subcoronary implantation and aortic root replacement was 4.8% (4 patients) and 4.2% (3 patients), respectively. The causes of death were cardiac failure unrelated to allograft valve failure. The overall survival rate by Kaplan-Meier analysis at 5 years was 81% (n = 8 deaths; 95% confidence interval, 72% to 89%) after subcoronary implantation and 94% (n = 4 deaths; 95% confidence interval, 92% to 97%) after aortic root replacement. The 5-year freedom from reoperation for allograft failure after subcoronary implantation and aortic root replacement was 86% (n = 10; 95% confidence limits, 82% and 90%) and 93% (n = 2; 95% confidence limits, 88% and 98%), respectively. These differences, evaluated with the log-rank test, were not significant (p > 0.05).

The median duration of follow-up for the hospital survivors was 4.2 years (range, 1 month to 7.7 years) after subcoronary implantation and 2.1 years (range, 1 month to 6.3 years) after aortic root replacement.

Echocardiographic methods
Between 1987 and 1993, the morphology and the function of the allograft aortic valves were assessed by serial precordial echocardiography. The peak velocity across the allografts was measured with continuous-wave Doppler in the apical view.

The pattern of the regurgitant jet was reviewed in the parasternal long-axis and short-axis views and in the four-chamber apical view. Aortic regurgitation was assessed by the jet length method on a scale of 0 to 4, and the data from patients with grade 2 aortic regurgitation or higher were used to describe the jet patterns after allograft implantation. These regurgitant jets extended into the left ventricular outflow tract sufficiently to allow analysis.

The echocardiographic examinations were performed on a Vingmed CFM 750 ultrasound system (Vingmed, Trondheim, Norway). The flow velocity was set between 0.7 and 1.0 m/s, depending on the depth. The threshold of the flow velocity was always set at 0.25 m/s.

Echocardiographic follow-up
For analysis of the pathomorphology, echocardiograms scored by the jet length method were available for 79 patients who underwent subcoronary implantation with a median interval after operation of 3.5 years (range, 2 months to 6.8 years). In the group having aortic root replacement, an echocardiogram was available for 57 patients with a median follow-up of 1.8 years (range, 4 months to 5.3 years). Unavailable for echocardiographic analysis were 6 patients who died in the hospital, 3 patients who were lost to follow-up, and 2 patients with an incomplete echocardiographic examination. For 5 patients who had operation recently, no echocardiogram was available.

Statistical analysis
Survival and freedom from reoperation for allograft failure were analyzed according to the Kaplan-Meier method [14]. The differences between curves were evaluated with the log-rank test. The unpaired t test was used to look for differences in peak velocity across the valves. A p value of less than 0.05 was considered significant.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Allograft stenosis
For the entire group of patients, the mean value of the peak velocity across the allograft aortic valve after subcoronary implantation was 1.8 m/s (range, 1.1 to 6 m/s) and after root replacement, 1.4 m/s (range, 1.0 to 2.1 m/s). This difference was not significant (p > 0.5). The reported peak velocity across the normally functioning native aortic valve is 1.3 m/s (range, 1.0 to 1.7 m/s) [15].

After subcoronary implantation, 4 patients (5%) had a pathologic gradient across the valve. One patient had reoperation for aortic stenosis 3.6 years after allograft implantation. On visual inspection, the explanted allograft valve showed severe calcified deposits on the leaflets. Another patient has moderate aortic stenosis (peak velocity of 2.6 m/s) and is in New York Heart Association class I after 5.6 years of follow-up. Combined aortic stenosis and regurgitation was observed in 2 patients. The valvular stenosis was caused by inward displacement of the allograft annulus resulting from dehiscence at the suture line with paravalvular regurgitation.

After root replacement, no pathologic gradients were encountered.

Paravalvular leakage and pseudoaneurysm
Paravalvular leakage was defined as a perfused space between the native aortic wall and the allograft. Typically, the onset of turbulent flow on color Doppler occurred during diastole between the proximal and distal suture lines (Fig 1).



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Fig 1. Postoperative color Doppler echocardiogram in parasternal long-axis view after subcoronary implantation of allograft aortic valve. The asterisk indicates the paravalvular leak. Turbulent flow was detected during diastole between the native aortic wall and the allograft. A small, centrally originating regurgitant jet is also present. (Ao = aorta.)

 
During echocardiographic follow-up, one or more paravalvular leaks were detected in 15% (12/79) of patients who had subcoronary implantation. Four of these patients had reoperation for severe paravalvular leakage. Two of them, who had combined aortic stenosis and regurgitation have been mentioned already. In the 2 others, the paravalvular leak was caused by dehiscence of sutures, but no stenosis was observed. One patient with a small paravalvular leak had a subannular mycotic aneurysm, which caused systolic compression of the left coronary artery. This patient required reoperation for intermittent ischemia. In the remaining 7 patients, the paravalvular leakage was not of hemodynamic importance, and no progression in severity has been observed during a mean follow-up of 5.2 years (range, 3.8 to 7.4 years). No paravalvular leaks were detected in the group with aortic root replacement.

Pseudoaneurysm was defined as an echo-free space between the aortic allograft and the native aortic wall and was encountered in 4 patients (3%) in the study. Pseudoaneurysms are due to partial dehiscence at the proximal or distal suture line. A pseudoaneurysm at the proximal anastomosis after root replacement was detected in 2 patients with Marfan’s disease (Fig 2). On color Doppler echocardiography, there was late diastolic turbulent flow. Both patients underwent reoperation. In 2 patients with subcoronary implantation, a supraannular pseudoaneurysm was detected at the distal suture line. On color Doppler echocardiography, diastolic flow was detected between the allograft wall and the native wall, but no continuity of this turbulence into the left ventricular outflow tract was seen. One of these patients had reoperation for aortic regurgitation, and dehiscence of the distal suture line was confirmed on visual inspection. The other patient is in New York Heart Association class I at 2.2 years of follow-up.



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Fig 2. Postoperative epicardial two-dimensional echocardiogram in parasternal long-axis view after allograft root replacement. The arrow points to a pseudoaneurysm at the proximal anastomosis. (Ao = aorta; Lv = left ventricle.)

 
Jet pattern
To investigate the influence of the allograft implantation technique on jet morphology, transvalvular aortic regurgitant jets were examined according to their jet pattern. These jets were found in 30 (38%) of 79 available echocardiograms after subcoronary implantation and in 3 (5%) of 57 available echocardiograms after aortic root replacement.

In the subcoronary implantation group, a central jet origin was found in 24 valves (80%) and a commissural origin in six valves (20%). Of the 30 regurgitant jets, 12 (40%) had a noneccentric trajectory and were directed centrally into the left ventricular outflow tract. An eccentric jet pattern was observed in 18 patients (60%). Fourteen jets were directed to the ventricular surface of the anterior mitral valve leaflet and four, to the interventricular septum. In patients with subcoronary implantation, no relation was found between jet direction and resection or preservation of the noncoronary sinus.

In the 3 patients who had aortic root replacement, the regurgitant jets originated centrally from the aortic valve. One jet had an eccentric trajectory and was directed to the anterior mitral valve leaflet. The other two jets had a central trajectory into the left ventricular outflow tract.

During the analysis, two possible confounding factors for semiquantitative assessment of aortic regurgitation in allografts were identified. First, 11 of the 24 jets with a central origin were directed toward a commissure, and on the parasternal short-axis view, the regurgitant jet was oval. These jets started with an intravalvular trajectory before they hit the left ventricular outflow and projected into the left ventricular outflow tract. Second, multiple regurgitant jets were seen in 7% (10/136) of the patients.


    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Two-dimensional echocardiography and color Doppler echocardiography are essential, noninvasive tools for the follow-up of patients with an allograft aortic valve. Serial postoperative examinations should detect early and late allograft failure because subcoronary implantation is prone to technical error and long-term durability of allografts is limited [15, 710, 16]. Proper interpretation is essential for the decision on whether to reoperate. Echocardiography has a great potential as a research tool to answer many relevant questions, such as the preferred implantation technique and the influence of donor-recipient interactions and allograft preservation methods on valve degeneration [10, 11, 17]. For this purpose, routine echocardiographic follow-up examinations may not be sufficient [10]. For patient counseling and research, allograft-specific pathology on cross-sectional and color Doppler echocardiography should be recognized but has drawn limited attention to date.

This study confirms previous echocardiographic observations on the favorable low transvalvular gradients of aortic allografts after subcoronary implantation and root replacement [3, 57, 9]. In our experience, there is a significantly higher incidence of reoperation for aortic regurgitation and stenosis after subcoronary implantation than after root replacement.

Oechslin and colleagues [12] studied the pathomorphologic findings with the current echocardiographic techniques after allograft aortic valve implantation. They described pseudoaneurysms in 73% (22/30) of patients after subcoronary implantation and root replacement. Root replacement was performed as an inclusion cylinder and, in some patients, as a freestanding root. No cases of paravalvular leakage were reported. In contrast, we detected a pseudoaneurysm at the proximal or distal anastomosis in 3% of all allograft patients. In the patients with root replacement and Marfan’s disease, we did not await further progression and performed a reoperation, although the aortic valve was competent. One patient with a pseudoaneurysm at the distal suture line after subcoronary implantation required reoperation for aortic regurgitation. As expected, paravalvular leaks occurred only after subcoronary implantation in 15% of our patients, but reoperation for aortic regurgitation or mixed valve disease was required in 5%. In only 1 patient were the sequelae of acute infective endocarditis not completely abolished by subcoronary allograft implantation, and a residual subannular mycotic aneurysm persisted. The difference in the incidence of echo-free spaces around allografts on echocardiography in the study of Oechslin and associates [12] and our study (73% versus 13%) can only in part be explained by different implantation techniques.

In this study, the morphology of jet patterns on color Doppler echocardiography was analyzed to detect differences between the subcoronary implantation technique with resection of all three sinuses of Valsalva compared with the technique of Ross [13], in which the noncoronary sinus is preserved. There were no differences in incidence or jet direction between the two techniques. We assume that jets originating centrally and projecting centrally into the left ventricular outflow tract are the result of a suboptimal match between host annulus and donor size. The most striking observation was the difference in incidence of eccentric jets between subcoronary implantation and root replacement. This finding supports the concept that the advantage of root replacement is better preservation of the geometry of the donor leaflets with less turbulent flow during closure. However, the learning curve might have influenced these results. It is unclear whether this finding has consequences for late valvular function.

The relevance of eccentric jets for the quantification of aortic regurgitation has been noticed previously by Jaffa and coworkers [5]. They found a 30% incidence of sharply angulating jets in allografts. In our study, there was a particularly high incidence of centrally originating jets, with an initial eccentric trajectory at the level of the leaflets that hit the left ventricular outflow wall and thereafter projected into the left ventricle. This occurred more commonly in subcoronary implanted allografts (11/24 or 46%). In addition, with multiple jets, an eccentric jet pattern may have confounding consequences for the quantification of aortic regurgitation after subcoronary implantation. These factors require more than routine attention during assessment of echocardiograms for the purpose of research.

We conclude that allograft-specific pathology on echocardiography, such as pseudoaneurysm or paravalvular leaks and eccentric jets, are more common after subcoronary implantation of allografts. Analysis of jet patterns with color Doppler echocardiography supports the validity of the concept of preservation of the geometry of the aortic root after root replacement. Quantification of regurgitant jets may frequently be confounded by an eccentric pattern and multiple jets.


    Acknowledgments
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
This research was supported by grant 42.001 from the Netherlands Heart Foundation. We gratefully acknowledge the secretarial assistance of Ada Matser-van den Berg.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. O’Brien M.F., McGiffin D.C., Stafford E.G., et al. Allograft aortic valve replacement: long-term comparative clinical analysis of the viable cryopreserved and antibiotic 4°C stored valves. J Cardiac Surg 1991;6(Suppl 4):534-543.[Medline]
  2. O’Brien M.F., Stafford E.G., Gardner M.A.H., et al. Allograft aortic valve replacement: long-term follow-up. Ann Thorac Surg 1995;60:S65-S70.
  3. Kirklin J.K., Smith D., Novick W., et al. Long-term function of cryopreserved aortic homografts. J Thorac Cardiovasc Surg 1993;106:154-166.[Abstract]
  4. Yacoub M., Ramsi N.R.H., Sundt T.M., et al. Fourteen-year experience with homovital homografts for aortic valve replacement. J Thorac Cardiovasc Surg 1995;110:186-194.[Abstract/Free Full Text]
  5. Jaffa W.M., Coverdale A., Roch A.H.G., et al. Doppler echocardiography in the assessment of the homograft aortic valve. Am J Cardiol 1989;63:1466-1470.[Medline]
  6. Jones E.L., Shah V.B., Shanewise J.S., et al. Should the freehand allograft be abandoned as a reliable alternative for aortic valve replacement?. Ann Thorac Surg 1995;59:1397-1404.[Abstract/Free Full Text]
  7. Daicoff G.R., Botero L.M., Quintessenza J.A. Allograft replacement of the aortic valve versus the miniroot and valve. Ann Thorac Surg 1993;55:855-859.[Abstract]
  8. Knott-Craig C.J., Elkins R.C., Stelzer P.L., et al. Homograft replacement of the aortic valve and root as a functional unit. Ann Thorac Surg 1994;57:1501-1506.[Abstract]
  9. Rubay J.E., Raphael D., Sluysmans T., et al. Aortic valve replacement with allograft/autograft: subcoronary versus intraluminal cylinder or root. Ann Thorac Surg 1995;60:S78-S82.
  10. Willems T.P., van Herwerden L.A., Steyerberg E.W., et al. Subcoronary implantation or aortic root replacement for human tissue valves: sufficient data to prefer either technique?. Ann Thorac Surg 1995;60:S83-S86.
  11. Willems T.P., van Herwerden L.A., Steyerberg E.W., et al. Echocardiographic follow-up study after free-hand aortic allograft or root replacement with aortic allograft/pulmonary autograft [Abstract]. Circulation 1996;94(Suppl 1):721.
  12. Oechslin E., Carrel T., Ritter M., et al. Pseudoaneurysm following aortic homograft: clinical implications?. Br Heart J 1995;74:645-649.[Abstract/Free Full Text]
  13. Ross D. Technique of aortic valve replacement with a homograft: orthotopic replacement. Ann Thorac Surg 1991;52:154-156.[Abstract]
  14. Kaplan E.L., Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc 1958;53:457-481.
  15. Hatle L., Angelson B. Doppler ultrasound in cardiology, 2nd ed. Philadelphia: Saunders, 1984:1110.
  16. Barratt-Boyes B.G., Roch A.H.G., Subramanyan R., Pemberton J.R., Whitlock R.M.L. Long-term follow-up of patients with the antibiotic-sterilized aortic homograft valve inserted free-hand in the aortic position. Circulation 1987;75:768-777.[Abstract/Free Full Text]
  17. Willems T.P., Bogers A.J.J.C., Cromme-Dijkhuis A.H., et al. Allograft reconstruction of the right ventricular outflow tract. Eur J Cardiothorac Surg 1996;10:609-615.[Abstract]



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