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Ann Thorac Surg 1999;68:1302-1307
© 1999 The Society of Thoracic Surgeons


Original Articles: Cardiovascular

Aortic root replacement with the pulmonary autograft: an invariably competent aortic valve?

Karl M. Dossche, MDa, Aart Brutel de la Riviére, MD, PhDa, Wim J. Morshuis, MD, PhDa, Marc A.A.M. Schepens, MD, PhDa, Sjef M. Ernst, MDb, Jurriaan J. van den Brand, MDa

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

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


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. Pulmonary autograft aortic root replacement was used in adults. Risk factors for aortic regurgitation (AR), and for pulmonary allograft valve stenosis are identified.

Methods. From February 1991 through April 1998, 80 adults (mean age 34.4 years) underwent pulmonary autograft aortic root replacement. Primary diagnosis was AR in 43 (53.7%) patients, aortic stenosis in 13 (16.3%) and mixed disease in 24 (30%) patients. A root reinforcement ring was used in 32 (40%) patients.

Results. There was no hospital mortality. Estimated patient survival is 100% at 7 years. A total of 3 patients underwent reoperation: 2 on the autograft for severe AR, 1 for pulmonary allograft stenosis. Freedom from reoperation on the autograft is 96.7 ± 2.4% at 7 years. Multivariate analysis indicated bicuspid aortic valve disease as an incremental risk factor for AR at discharge (p = 0.036, odds 3.5). Univariate analysis identified operation for pure AR as risk factor for AR during follow-up (p = 0.041). Mild AR or more increased from 2.5% at discharge to 11.3% during follow-up (p = 0.008). Progression of AR was limited by the use of a reinforcement root ring (p = 0.031). Freedom from mild AR or more in patients with and without a reinforcement root ring was 100% and 72.9 ± 9.3% respectively, at 5 years (p = 0.119). Pulmonary allograft stenosis occurred in 15 (22.5%) patients. Multivariate analysis revealed that large sized pulmonary allografts were less prone to stenosis (p = 0.048, odds 0.13).

Conclusions. Pulmonary autograft root replacement can be performed with few complications. During follow-up, a significant increase in mild AR or more is observed. The use of a reinforcement root ring is effective in preventing progression of AR.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The use of the autologous pulmonary valve to replace the aortic valve in a human being was first described by Ross in 1967 [1]. His initial clinical experience was with intraaortic implantation of the autograft in the subcoronary position after scalloping its sinuses. Long-term results of the pioneer series showed that reoperation was ultimately necessary in 30 of 131 hospital survivors (23%) for severe regurgitation of the autograft [2]. In efforts to improve the compliance rate, techniques other than the original subcoronary implantation have been used. These techniques include the use of the pulmonary autograft as an intraluminal cylinder or as a freestanding root [3, 4]. In this report we describe our experience in replacing the aortic root with a pulmonary autograft in 80 adults with aortic valve disease and the results of serial echocardiographic studies, assessing the function of these autografts and of the pulmonary allografts that were implanted in the right ventricular outflow tract (RVOT).


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
From February 1991 through April 1998, 80 patients underwent aortic valve and root replacement with the pulmonary autograft with three responsible surgeons. Demographic and preoperative cardiac variables are summarized in Table 1. Patients were aged 16 to 56 years (mean 34.4 ± 9.3 years) and showed the usual male predominance and range of aortic valve pathology. The patients were free from important comorbidity and generally had good left ventricular ejection fraction.


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Table 1. Preoperative Details of the 80 Patients in the Series

 
Preoperative evaluation
All patients underwent preoperative left-heart catheterization and coronary angiography to assess the severity of the aortic valve disease, left ventricular ejection fraction and to disclose the anatomy of the coronary arteries and the septal perforating branches of the anterior descending coronary artery. Transthoracic two-dimensional echocardiography for size estimates of the aortic and pulmonary annulus was not included routinely in the preoperative evaluation.

Operative procedure
The technique for excision of the pulmonary root and its implantation into the aortic root have been described [4, 5]. Standard cardiopulmonary bypass techniques including high aortic and bicaval cannulation and moderate systemic hypothermia were used in all patients. The myocardium was protected by low sodium normopotassic cardioplegic solution directly into the coronary ostia and continuous external cooling with 4°C crystalloid solution. The sequence of the operation was as follows: excision of the diseased aortic valve; inspection and excision of the patient’s own healthy pulmonary valve; proximal insertion of the pulmonary autograft into the aortic root; reimplantation of both coronary ostia as free buttons; first, distal, and then proximal reconstruction of the RVOT with a pulmonary allograft; and finally end-to-end anastomosis between the distal pulmonary autograft and native aorta. For the proximal pulmonary autograft insertion, a continuous suture technique with three 4-0 polypropylene sutures was used in all patients. The diameter of the aortic annulus and pulmonary autograft was assessed only by intraoperative measurement with cylindrical sizers. Reinforcement of the proximal suture line with fresh autologous pericardium or prosthetic material (Teflon felt, Impra Inc, subsidiary of C.R. Bard, Tempe, AZ, or a woven Dacron ring, C.R. Bard, Haverhill, PA) was performed in 32 (40%) patients. In case of pericardium or Teflon felt, the ring was made restrictive by sewing each end, end-to-end, to prevent stretching. In 5 patients a reduction annuloplasty was performed because the aortic annular diameter exceeded the Z+2 value for the body surface area (two standard errors above the expected normal size predicted for the body surface area) [68]. Two 2-0 polypropylene sutures were placed as purse-string sutures in the aortic annulus, 2 mm apart, at the nadir of the coronary sinus, and continuing in a single plane below the aortic annulus in the interleaflet triangle below the commissures. The RVOT was reconstructed with a cryopreserved pulmonary allograft in 79 patients, and with a bovine pericardium mounted xenograft in 1 patient. Proximal and distal anastomosis were performed each with a single continuous 5-0 or 6-0 polypropylene suture. A reduction aortoplasty was necessary in 10 (12.5%) patients for incongruence between the distal pulmonary autograft and the residual ascending aorta. Other concomitant procedures included mitral valve plasty in 1 patient and open mitral commissurotomy in 1. One patient with single-vessel coronary artery disease underwent a PTCA 3 days before the autograft procedure. Mean cardiopulmonary bypass (ECC) time was 180 ± 33 minutes (range 135–285), mean aortic cross-clamp (CC) time was 130 ± 21 minutes (range 98–200).

Pulmonary allograft data
All cryopreserved allografts for RVOT reconstruction were provided by Bio Implant Services Foundation (BIS), Leiden, The Netherlands. The donors varied in age from 9 to 66 years (mean 44.7 ± 13.5 years). Dissection of the heart was generally performed within 24 hours after circulatory arrest. Following dissection, the valves were decontaminated by incubation for 5 to 6 hours at 37°C in a medium containing an antibiotic mixture (ciprofloxacin, amikacin, metronidazole, vancomycin, flucytoxin). Thereafter, valves were cryopreserved in medium containing 10% dimethylsulfoxide 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 donors were seronegative for human immunodeficiency antibodies, hepatitis B surface and core antigen, hepatitis C antibodies, and treponema pallidum (hemagglutination). Details are listed in Table 2.


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Table 2. Characteristics of Pulmonary Allografts Used for Reconstruction of the RVOT (n = 79)

 
Postoperative follow-up
The end of the study period was set at June 1998, by which time subjects had been followed up for 84 months (median 24 months). Of the 80 patients, 79 (98.5%) were identified to this date, representing 188.5 patient-years. Data were collected from the patients’ cardiologists or from our own cardiology department. Assessment included New York Heart Association functional class, drug therapy, electrocardiogram, chest radiogram, and transthoracic M-mode, two-dimensional, color-flow, and Doppler echocardiograms. The presence of regurgitation in the autograft and the allograft was determined by continuous-wave, pulsed-wave, and color-flow Doppler methods. Regurgitation was graded on a scale from 0 to IV. A valve with no regurgitation was graded as 0, trivial regurgitation as I, mild incompetence as II, moderate incompetence as III, severe regurgitation as IV. Evidence of obstruction of blood flow was detected by measurement of peak velocity of the flow across the pulmonary autograft or pulmonary allograft [9]. Valve stenosis was graded as present when blood velocity across the valve exceeded 1.4 m/s.

Statistical analysis
The time-related events of interest included death after hospital discharge, reoperation on the autograft valve or pulmonary position valve, endocarditis, and thromboembolic incidents. In all analyses, time zero was the time of the original autograft operation. Nonparametric estimates of the non-risk adjusted distribution of the time interval to the various events were obtained by the method of Kaplan and Meier [10]. Comparison of survival groups was made using the log rank test.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Mortality and morbidity
There were no hospital deaths. Seven (8.9%) patients required early (< 24 hours) reoperation for bleeding; EEC was not necessary in any of them. Three (3.8%) patients sustained myocardial damage (creatinine phosphokinase > 300 IU/l, myocardial band > 5%); 1 of them underwent coronary angiography and stenting of an ostial stenosis of the reimplanted right coronary artery. Three (3.8%) patients required a permanent pacemaker for permanent total atrioventricular block. One of those 3 was a reoperation and the other 2 required debridement of extensive calcification involving the membranous septum and the adjacent muscular septum. There have been no deaths during the follow-up period, which at this writing extends to 84 months (median follow-up 24 months); nor have there been any episodes of thromboembolism or infective endocarditis. Two reoperations have been required on the autograft valves 1 and 15 months after the initial procedure for severe aortic regurgitation (AR). In 1 patient, the pulmonary autograft was quadruspid, which had been discovered only at the end of the initial operation; in another patient the cause for autograft failure was unclear. In both patients, a mechanical prosthesis was implanted inside the pulmonary autograft. Estimated freedom from reoperation on the pulmonary autograft is 96.7 ± 2.4% at 7 years. One 17-year-old patient required reoperation for stenosis of the pulmonary allograft 13 months after the initial operation. The stenosis was confined to the annulus of the allograft valve and was relieved using a patch of bovine pericardium. Estimated freedom from reoperation on the pulmonary allograft is 98.1 ± 1.8 % at 7 years. Estimated freedom from reoperation for any cause is 94.9 ± 2.9% at 7 years.

Echocardiographic studies
Pulmonary autograft function
A two-dimensional echocardiographic study was performed in all patients within 6 weeks after the operation (range, 7 to 41 days). There was no AR in 58 (72.5%) patients; 20 (25%) patients had trivial regurgitation; 1 (1.25%) had mild regurgitation; and 1 (1.25%) had severe regurgitation requiring reoperation 6 weeks after the autograft procedure. Fourteen (63.5%) of these patients had a native bicuspid aortic valve, 8 of them had a primary diagnosis of pure AR. Regurgitation was central in the majority of patients. The influence of variables, including age, gender, preoperative AR, bicuspid valve, diameter of aortic annulus, reduction aortoplasty, history of acute rheumatic fever, and use of a root ring on the incidence of postoperative AR was investigated. At univariate analysis, none of these variables showed significance at a level of 0.05. Stepwise logistic regression identified bicuspid native aortic valve as the only independent risk factor associated with AR at discharge (p = 0.036, odds 3.5). During follow-up, echocardiographic data 64 patients were available. Excluded were 12 patients with a follow-up of less than 1 year, 3 patients without a recent echocardiographic study, and 1 patient who underwent reoperation within the first year after the autograft procedure. Aortic regurgitation was absent in 42 (65.6%) patients; 15 (23.4%) had trivial AR; 6 (9.2%) had mild AR; and 1 (1.8%) had severe AR requiring reoperation 15 months after the autograft procedure. None of the patients had aortic valve stenosis. Details are listed in Table 3. Kaplan-Meier estimated freedom from mild or more AR was 77.5 ± 8.5% at 7 years (Fig 1). The difference in occurrence of AR (grades I to IV) at discharge and during follow-up was not significant (p = 0.653); however, a significant increase in mild or more AR was observed during follow-up: 2.5 % at discharge versus 11.3% during follow-up (p = 0.008). The same variables analyzed for their influence on AR at discharge were studied for their influence on AR during follow-up. At univariate analysis, operation for pure AR was the only factor associated with AR during follow-up (p = 0.041). Multivariate analysis failed to recognize variables influencing during follow-up. Eleven patients developed AR or had progression of their AR during follow-up; 8 of them had a preoperative diagnosis of (p= 0.137). In only 1 of 11 patients was a reinforcement root ring used (p = 0.031). At univariate analysis, the use of a root ring (autologous pericardium or prosthetic) was the only (protective) factor associated with progression of AR during follow-up. Kaplan-Meier freedom from mild AR or more in patients with a reinforcement root ring is 100 %, in patients without reinforcement ring 72.9 ± 9.3%, both at 5 years (log rank p = 0.119)(Fig 2). Using Cox proportional hazard model, AR at discharge was the only independent risk factor associated with progression of aortic insufficiency (p = 0.047, odds 4.5).


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Table 3. Details of Aortic Valve Function Assessed by Transthoracic Echocardiography in Patients With > 1 Year Follow-up (n = 64)

 


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Fig 1. Overall freedom from aortic regurgitation (AR) grade II/IV or more during follow-up (dotted lines indicate 70% confidence limits).

 


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Fig 2. Freedom from AR grade II/IV or more during follow-up with and without the influence of a reinforcement root ring.

 
Pulmonary allograft function
None of the patients had pulmonary valve stenosis at discharge, 5 (6.3%) patients had trivial pulmonary regurgitation. During follow-up, pulmonary allograft stenosis (peak velocity across the pulmonary allograft > 1.4 m/s, gradient > 20 mm Hg) occurred in 15 patients (22.5%). One patient required reoperation on the pulmonary allograft for a stenosis of more than 50 mm Hg, although this was clinically well tolerated. The influence of diameter and age of the pulmonary allograft, donor status, time between cardiocirculatory arrest and dissection of the valve, time between circulatory arrest and cryopreservation, and age of recipient was studied on the development of pulmonary allograft valve stenosis. Univariate analysis indicated that allografts with an internal annular diameter greater than 27 mm were less prone to pulmonary valve stenosis (p = 0.027). Using the Cox proportional hazard model, this was the only significant variable during follow-up which had a negative influence on the development of pulmonary valve stenosis (p = 0.049, odds 0.13). Kaplan-Meier freedom from pulmonary allograft valve stenosis with a transvalvular gradient greater than 20 mm Hg at 7 years was 39.8 ± 13.4%; freedom from pulmonary allograft stenosis with a transvalvular gradient greater than 30 mm Hg was 75.5 ± 13.3% at 7 years (Fig 3).



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Fig 3. Freedom from pulmonary allograft valve stenosis during follow-up.

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Ross conceived the pulmonary autograft procedure, hoping to create an aortic valve replacement close to the ideal [1]. A 10% surgical mortality during the initial phase of the development of the operation, and concerns regarding the ability of the pulmonary valve to withstand the hemodynamic stress of the aortic position, dissuaded surgeons from using this operation for aortic valve replacement, when other standard valve replacement operations could be applied with a risk of 2% to 5%. The more recent surgical mortality is less than 5% [1113]. Kouchoukos reported no surgical mortality in 33 patients who underwent replacement of the aortic root with a pulmonary autograft, Stelzer reported an early mortality of 4.8 % in 145 patients [11, 12]. In a selected group of patients (upper age limit 56 years), we observed no surgical mortality. All operations were done electively, the majority of them in patients without the need for time-consuming concomitant procedures. Patients with concomitant extensive coronary disease were not considered for this type of operation; in case of single-vessel or two-vessel disease, a PTCA was performed a few days before surgery. We do not feel that the application of the Ross procedure should be extended to patients with acute endocarditis with extensive aortic root abscesses. This procedure opens more tissue planes and adds excessive operating time for patients in whom sepsis syndrome will persist for several hours after the operation. Moreover, the aortic allograft is usually provided with the donor anterior mitral leaflet, which may be very helpful in the reconstruction of the aorto-mitral continuity. We prefer aortic root replacement with a cryopreserved allograft in this setting [14].

Over the last few years, the implantation techniques have been addressed. Longest experience exists with the implantation in the subcoronary position. In an extensive analysis of the late results of 131 hospital survivors with a mean follow-up of 20 years, Chambers and associates reported 30 (23%) reoperations for severe AR. Freedom from replacement of the autograft in the subcoronary position at 20 years was 78%; the majority (75%) of patients alive were free from significant regurgitation [2]. These findings are consistent with other reports of the same group on the pulmonary autograft in the subcoronary position [15, 16]. Elkins and associates demonstrated a significant advantage of the freestanding aortic root over the inclusion cylinder and subcoronary technique with severe AR and reoperation as criteria, with however, a considerably shorter median follow-up of 2.4 years [17]. The results of our study are consistent with the results of other reports using the pulmonary autografts as a freestanding root [11, 12]. The incidence of reoperation on the autografts is absent or low, and the presence of more than trivial AR is in the range between 10% and 20%. These results seem favorable when compared to the subcoronary technique, but follow-up is considerably shorter. Whether or not these initial encouraging results will persist over the years is still unclear. Uncertainty regarding the use of a freestanding root concerns the possibility of stretch or distention of the root under systemic pressure, and the potential for dilatation of the pulmonary artery. The demonstration in our study of the increased risk for autograft regurgitation in patients with bicuspid aortic valve disease or preoperative diagnosis of pure AR has been recognized by others [17, 18]. A matter of concern in our series is the observed progression of mild AR or more over a relatively short period of follow-up. Analysis of the results indicated that this was almost exclusively in patients with a preoperative diagnosis of AR, and in whom a reinforcement root ring was not used. As diameters at various levels were not systematically measured, we can not determine from our study whether or not the progression of AR is due purely to dilatation at the annular level or also sited at the level of the sinotubular junction. Reinforcement of the aortic annulus or adjustment of the diameter of the aortic annulus to that of the pulmonary autograft have been recommended for prevention of AR [6, 17, 18]. Initially we did not consistently use any of these techniques; more recently however, we invariably use a reinforcement ring or a reduction annuloplasty as described by Carpentier in all situations of annular dilatation. Over a 5-year follow-up interval, the protective effect of the reinforcement root ring on progression of AR was already clearly present.

RVOT reconstruction was routinely done with a cryopreserved allograft in our series. In this report as well as in others, cryopreserved pulmonary allografts were the conduit of choice [24, 11, 12]. We and others have observed a significant increase in pulmonary flow velocities during follow-up [2, 12]. Pulsed wave Doppler demonstrated that the gradient was located directly at the allograft leaflets and not at the anastomosis. Increased flow velocities are therefore valve related and stiffness of the allograft leaflets or allograft wall decrease the valve opening. Based on the data of our multivariate analysis, we recommend the use of large pulmonary allografts for RVOT reconstruction. The need for the right-sided pulmonary allograft to be replaced at least once in the very young remains a problem, but this operation can usually be performed with low risk to the patient.

The initial results of freestanding aortic root replacement with the pulmonary autograft are good. Even with this technique, AR is frequently observed, although trivial or mild in the majority of cases. Measurements to prevent AR or progression of AR are recommended in situations of bicuspid aortic valve disease and preoperative AR.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Ross D.N. Replacement of aortic and mitral valves with a pulmonary autograft. Lancet 1967;2:956-958.[Medline]
  2. Chambers J.C., Somerville J., Stone S., Ross D.N. Pulmonary autograft procedure for aortic valve disease. Long-term results of the pioneer series. Circulation 1997;96:2206-2214.[Abstract/Free Full Text]
  3. Elkins R.C., Santangelo K.L., Stelzer P., Randolph J.D., Knott-Craig C.J. Pulmonary autograft replacement of the aortic valve. J Card Surg 1992;7:108-116.[Medline]
  4. Stelzer P., Jones D.J., Elkins R.C. Aortic root replacement with pulmonary autograft. Circulation 1989;80(Suppl):III209-III213.
  5. Ross D.N. Replacement of the aortic valve with a pulmonary autograft. Ann Thorac Surg 1991;52:1346-1350.[Abstract]
  6. Elkins R.C., Knott-Craig C.J., Howell C.E. Pulmonary autografts in patients with aortic annulus dysplasia. Ann Thorac Surg 1996;61:1141-1145.[Abstract/Free Full Text]
  7. Roman M.J., Devereux R.B., Kramer-Fox R., O’Loughlin J. Two-dimensional echocardiographic root dimensions innormal children and adults. Am J Cardiol 1989;64:507-512.[Medline]
  8. Carpentier A. Cardiac valve surgery—the "French correction.". J Thorac Cardiovasc Surg 1983;86:323-337.[Medline]
  9. Currie P.J., Seward J.B., Reeder G.S., Vlietsra R.E. Continuous wave Doppler echocardiographic assessment of severity of calcific aortic stenosis. Circulation 1985;71:1162-1169.[Abstract/Free Full Text]
  10. Kaplan E., Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc 1958;53:457-481.
  11. Kouchoukos N.T., Davilla-Roman V.G., Spray T.L., Murphy S.F., Perillo J.B. Replacement of the aortic root with a pulmonary autograft in children and young adults with aortic valve disease. N Engl J Med 1994;330:1-6.[Abstract/Free Full Text]
  12. Stelzer P., Weinrauch S., Tranbaugh R.F. Ten years experience with the modified Ross procedure. J Thorac Cardiovasc Surg 1998;115:1091-1100.[Abstract/Free Full Text]
  13. Hokken R.B., Bogers A.J., Taams M.A., et al. Aortic root replace-ment with a pulmonary autograft. Eur J Cardiothorac Surg 1995;9:378-383.[Abstract]
  14. Dossche K., Brutel de la Riviére A., Morshuis W., Schepens M., Ernst J. Aortic root replacement with human tissue valves in aortic valve endocarditis. Eur J Cardiothorac Surg 1997;12:47-55.[Abstract]
  15. Ross D.N., Jackson M., Davies J. The pulmonary autograft—a permanent aortic valve. Eur J Cardiothorac Surg 1992;6:113-117.[Abstract]
  16. Matsuki O., Okita Y., Almeida R.S., et al. Two decades’ experience with aortic valve replacement with pulmonary autograft. J Thorac Cardiovasc Surg 1988;95:705-711.[Abstract]
  17. Elkins R.C., Lane M.L., McCue C. Pulmonary autograft reoperation. Ann Thorac Surg 1996;62:450-455.[Abstract/Free Full Text]
  18. David T.E., Omran A., Webb G., Rakowkski H., Armstrong S., Sun Z. Geometric mismatch of the aortic and pulmonary roots causes aortic insufficiency after the Ross procedure. J Thorac Cardiovasc Surg 1996;112:1231-1239.[Abstract/Free Full Text]
Accepted for publication April 4, 1999.




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