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Ann Thorac Surg 2007;83:1285-1289
© 2007 The Society of Thoracic Surgeons


Original Articles: Cardiovascular

The Ross Procedure: Clinical and Echocardiographic Follow-Up in 219 Consecutive Patients

Bruno Chiappini, MD, PhD*, Bruno Absil, MD, Jean Rubay, MD, PhD, Philippe Noirhomme, MD, Jean-Christophe Funken, MD, Robert Verhelst, MD, Alain Poncelet, MD, Gebrine El Khoury, MD

Department of Thoracic and Cardiovascular Surgery, Saint Luc Hospital, Université Catholique de Louvain, Brussels, Belgium

Accepted for publication November 21, 2006.

* Address correspondence to Dr Chiappini, Department of Thoracic and Cardiovascular Ssurgery, Saint Luc Hospital, Université Catholique de Louvain, avenue Hippocrate 10, 1200 Brussels, Belgium (Email: bruno_chiappini{at}hotmail.com).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: The replacement of the diseased aortic valve with a pulmonary autograft has been shown to provide excellent hemodynamic results and to be associated with low morbidity and mortality rates.

Methods: From 1991 to 2005, 219 patients undergoing the Ross operation were identified. All patients underwent transthoracic echocardiography at discharge and were scheduled for a yearly study thereafter. The echocardiographic study consisted of a morphologic analysis of the pulmonary autograft with measurement of end-systolic diameters at three levels: annulus, sinuses of Valsalva, and origin of the ascending aorta 2 cm above the sinotubular junction. The dynamic analysis evaluated the function of the aortic autograft and the pulmonary homograft. Maximal and mean aortic and pulmonary transvalvular pressure gradients were investigated.

Results: The 30-day mortality was 1.8% (n = 4). Cardiac deaths were not related to the autograft. The 10-year actuarial survival was 95.7% ± 2.1%. Six patients (2.8%) had grade 2 autograft valve regurgitation. No grade 3 or 4 pulmonary regurgitation was identified. At their most recent follow-up, 28 patients (13.1%) had grade 1 insufficiency of the pulmonary homograft, and 10 patients (4.6%) had a peak transvalvular gradient of 17.9 ± 10.2 mm Hg.

Conclusions: Our current experience suggests that replacement of the aortic root with a pulmonary autograft can be safely performed in infants, children, and adults and is associated with low mortality and morbidity rates. It constitutes an elegant alternative to the use of prosthetic valves in the treatment of aortic valve diseases.


    Introduction
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
The replacement of the diseased aortic valve by the pulmonary autograft, a procedure introduced by Donald Ross in 1967, has been shown to provide excellent hemodynamic results and to be associated with low morbidity and mortality rates [1–4]. The increased technical difficulty of this procedure and concerns about early and late failure initially led to its limited usage. With added experience, however, the advantages of the Ross procedure have become more fully appreciated. These include excellent hemodynamic performance, low endocarditis risk, low thrombogenicity, avoidance of anticoagulant therapy, and the assumed growth potential of the autograft valve in children [4–7].

The original implant technique, namely subcoronary freehand grafting, was associated with substantial prevalence of early and late valve dysfunction [8]. More recent experience with pulmonary autografts used for complete or partial aortic root replacement allowed for lower transvalvular gradients and fewer valvular regurgitations [4].

The long-term fate of the pulmonary homograft and aortic pulmonary autograft is largely unknown, particularly in adult patients. Concern has been growing over reports of progressive autograft root dilatation and valve dysfunction [9–14]; however, the exact magnitude of the phenomenon and its clinical consequences are still matter of controversy [15–18]. In the light of recent concern about progressive dilatation of the pulmonary autograft in the aortic position and growing evidence on the limited durability of the allograft in the right ventricular outflow tract, a retrospective analysis of all patients who underwent a Ross operation in our institution was performed.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
We identified 219 consecutive patients who underwent a Ross operation from July 1991 to December 2005. Demographic data are reported in Table 1. Our Institutional Review Board approved this study, and individual consent for the study was not required.


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Table 1 Preoperative Patient Characteristics a
 
Operative Techniques
Three operative techniques were used to implant the autologous pulmonary valve in the aortic position. The subcoronary technique was used for allografts during our early experience, followed by freestanding complete aortic root replacement and cylinder inclusion replacement. The latter two techniques currently represent the techniques of choice, root replacement being preferred in small (< 20 mm diameter) and large (> 8 mm diameter) annuli, and the inclusion cylinder preferred in adults.

Operations were performed under moderate hypothermia (28°C) at the beginning and later under normothermic cardiopulmonary bypass. Myocardial protection was achieved by antegrade warm cardioplegia. Approach to the aortic root was gained by a complete circumferential aortic transection, 2 cm above the sinotubular junction. After inspection of the pulmonary valve, the autograft was harvested within a cylinder of right ventricular outflow tract. The procedure was performed according to previously described techniques [1, 4, 10].

Buttressing of inflow (annular) and outflow (ascending aorta) suture lines with strips of glutaraldehyde-fixed autologous pericardium was used during freestanding root replacement to improve hemostasis. The right ventricular outflow tract was reconstructed with a cryopreserved pulmonary homograft (mean diameter, 24.9 ± 2.1 mm; range, 16 to 34 mm) in all but 3 patients, who received a porcine stentless xenograft.

Associated procedures were performed in 62 patients, including coronary artery bypass grafting in 9 (4.1%), reductive tailoring aortoplasty in 6 (2.7%), ascending aorta replacement in 23 (10.5%), atrial septal defect repair in 3 (1.4%), mitral valve replacement in 2 (0.9%), mitral valve repair in 16 (7.3%), and the Konno procedure in 3 (1.4%). The mean duration of cardiopulmonary bypass was 157.2 ± 28.7 minutes (range, 110 to 263 minutes), and the cross-clamping time was 129.5 ± 19.9 minutes (range, 93 to 201 minutes).

Postoperative Evaluation
All patients underwent transthoracic echocardiography at discharge and were scheduled for yearly examinations thereafter. The examinations were performed with 2.5-MHz ultrasound transducers (Sonos 2500 system, Hewlett-Packard, Palo Alto, CA). The echocardiographic study consisted of a morphologic analysis of the pulmonary autograft with measurement of end-systolic diameters at three levels: the annulus, sinuses of Valsalva, and origin of the ascending aorta 2 cm above the sinotubular junction. The dynamic analysis evaluated the function of the aortic autograft and the pulmonary homograft. The severity of regurgitation was classified according to four grades using classic semiquantitative criteria [19]. Maximal and mean aortic and pulmonary transvalvular pressure gradients were investigated. The mean duration of follow-up was 59.2 ± 40.8 months and was 93.6% complete (200/214 patients).

Statistical Analysis
The combined results of the collected data were analyzed using SPSS 13.0 (SPSS Inc, Chicago, IL) for Windows (Microsoft, Redmond, WA). Categoric variables are reported as absolute numbers and percentages. Continuous variables are expressed as means ± standard deviation. Comparison of continuous variables was performed using the two-tailed Student t test for paired data, and comparison of discrete variables was done with the Pearson {chi}2 test or Fisher exact, as appropriate. All tests were two-sided, with an {alpha}-level of 0.05.

Univariate logistic regression was used to study potential determinants of early mortality, defined as death during hospitalization or within 1 month after operation. The variables considered were patient age, prior cardiac surgery, New York Heart Association (NYHA) functional class, concomitant procedures, preoperative left ventricular function, and perfusion time. Study end points were survival, freedom from autograft dilatation, freedom from moderate or greater autograft regurgitation, and freedom from reoperation on the autograft.

Cumulative survival was analyzed using the Kaplan-Meier method. The survival of a patient started at the time of surgery and ended at death or at the last follow-up. For overall survival, the variables that were also considered for operative mortality were analyzed. The variables considered for freedom from reoperation or reintervention were patient age, diagnosis (regurgitation, stenosis, mixed), cause of the valve disease, prior cardiac surgery, and concomitant procedures. Multivariate analysis was performed using Cox proportional hazard method to identify risk factors for time-related occurrence of autograft dilatation and autograft regurgitation. Variables entered in the analysis were age, gender, diagnosis (regurgitation, stenosis, mixed), cause of the valve disease, prior aortic procedure, and associated procedures.


    Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Mortality
The 30-day mortality was 1.8% (n = 4). Cardiac deaths were not related to the autograft. The statistical analysis showed the reductive tailoring aortoplasty was associated with an increased risk of operative mortality (p = 0.006). One late death occurred during the follow-up as a result of a carcinoma. The 10-year actuarial survival was 95.7% ± 2.1% (Fig 1).


Figure 1
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Fig 1. Cumulative overall survival after Ross procedure.

 
Morbidity
Five patients (2.3%) required reoperation for bleeding. Acute renal insufficiency developed in 4 patients (1.8%). Two patients (0.9%) had an acute myocardial infarction, and a complete atrioventricular block developed in 2 patients (0.9%) that required the implantation of a permanent pacemaker. Atrial fibrillation requiring drug therapy occurred in 18 patients (8.2%), in which the ascending aorta had been replaced, this was a statistically significant risk factor (p = 0.03). Mean hospital stay was 12.7 ± 5.9 days (range, 5 to 38 days).

Late Clinical Outcome
A reoperation on the autograft was a required in 1 patient for a prolapse of the right coronary artery cusp 6 years after the Ross operation. Other than that, no adverse cardiovascular events were recorded in any of the patients during follow-up, including congestive heart failure, myocardial ischemia, hemorrhage, thromboembolism, or endocarditis. All surviving patients were in NYHA class I, and all resumed normal lifestyles, including regular schooling (children and adolescents) or employment (adults).

Echocardiographic Studies
Left ventricular function significantly improved after operation. We evaluated three variables preoperatively and at follow-up: the left ventricular telediastolic volume was 55.5 ± 9.1 mm versus 51.8 ± 7.5 mm (p < 0.001); the left ventricular index mass was 150.7 ± 52.6 g/m2 versus 108.5±32.3 g/m2 (p < 0.001); and the left ventricular ejection fraction was 64% ± 10% versus 68% ± 9% (p = 0.007).

No significant difference was noted between the mean values at discharge and the last follow-up concerning the aortic root diameters: the annulus was 25.5 ± 5.1 mm versus 27.4 ± 4.9 mm, the sinus of Valsalva was 34.2 ± 3.8 mm versus 35.6 ± 4.3 mm, and the ascending aorta was 28.3 ± 2.9 versus 31.7 ± 4.5 mm.

Grade 2 autograft valve regurgitation was found in 6 patients (2.8%; Fig 2). No grade 3 or 4 pulmonary regurgitation was identified. At their most recent follow-up, 28 patients (13.1%) were identified has having grade 1 insufficiency of the pulmonary homograft, and 10 patients (4.6%) had a peak transvalvular gradient of 17.9 ± 10.2 mm Hg.


Figure 2
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Fig 2. Actuarial freedom from grade 2 or greater autograft regurgitation.

 

    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Clinicians taking care of patients with significant aortic valve disease often face the difficult dilemma of when to operate and what graft material to implant. The choices usually are:
mechanical prostheses, which are long lasting but require anticoagulation, expose the patient to a continuous infectious risk [20], and may display suboptimal hemodynamic performance, particularly on exertion [20, 21];
• xenografts, which do not require anticoagulation but often exhibit worse hemodynamic performances than mechanical prostheses [22] and frequently degenerate, particularly in the young (23); and
• homografts, which also have limited durability, do not grow, and hence often require reoperation.

Since 1991, all patients at our institution with irreparable aortic valve disease and at least 20 years of predicted life expectancy have been offered pulmonary autograft valve replacement. Contraindications to the Ross procedure include prior cardiac surgery jeopardizing the integrity of the pulmonary autograft; recognized connective tissue disease, including Marfan syndrome, Ehlers-Danlos syndrome, and osteogenesis imperfecta; and chronic inflammatory disorders such as rheumatic heart disease and rheumatoid arthritis.

The Ross procedure was introduced in 1967 [1] as a possible alternative for aortic valve replacement. It is only recently, however, that the pulmonary autograft replacement of the diseased aortic valve is being performed more frequently by surgeons, probably because of the many technical difficulties inherent with this procedure and the unknown outcome of the double valve replacement. Despite these initial concerns, results of large-scale clinical studies indicated that this procedure was safe, with favorable short-term [8, 24, 25] and long-term results [8, 26]. The present data are thus in agreement with these earlier reports.

The hospital mortality in our series was 1.8% and comparable with the 2.5% reported in the International Ross Registry [27]. No patient in our series died late from valve-related complications. The only late death was caused by noncardiac events, reflecting the excellent survival of this operative technique. The overall survival rate at 10 years postoperatively was 95.7% ± 2.1%. Chambers and colleagues [8] reported a survival rate of 85% after 10 years and 61% after 20 years, whereas Elkins and colleagues [28] described a 10-year survival rate of 87% after the Ross procedure using the freestanding root technique in a group of patients with a mean age of 22 years (range, 1 week to 62 years). In addition, we did not observe any thromboembolic events or endocarditis, and also had an extremely low 0.5% incidence of reintervention. Several other studies have demonstrated a very low incidence of regurgitation requiring reintervention [4, 29–32].

Chambers and colleagues [8] reported the long-term results of Ross’ pioneer series of 131 hospital survivors operated at the National Heart Hospital, London, from 1967 to 1984 [8]. Freedom from autograft replacement was 88% at 10 years and 75% at 20 years, and freedom from replacement of the pulmonary position homografts was 89% at 10 years and 80% at 20 years. Elkins [33] reported 94% freedom from reoperation of the autograft and 90% freedom from reoperation of the homograft at 8 years. Freedom from autograft reoperation or dysfunction (3+ insufficiency) was 83% at 9 years [33].

In our study, with a maximum follow-up of 176 months, no patient was found to present with a peak transvalvular gradient exceeding 20 mm Hg at the level of the pulmonary autograft. These low peak gradients are very close to peak gradients seen in native valves and make the use of this surgical procedure highly feasible in young, active patients. In relation to the homograft, the peak transvalvular gradient at late follow-up remained entirely acceptable at 17.9 ± 10.2 mm Hg, which is close to that reported in other studies [32, 34–36].

Reoperation of the autograft was necessary in our series in 1 patient within 6 years after the operation because of right coronary leaflet prolapse. In concert with the stable function of the autograft over time, it becomes evident that the degeneration rate of the autograft seems to be low. The function of the autograft regarding the pressure gradient was excellent, simulating almost normal conditions in all patients.

The International Ross Registry reports that 86% of patients have aortic valve insufficiency of grade I or less, 9% have insufficiency grade II, 3% have insufficiency grade III, and 2% have grade IV. The completeness of the follow-up of the International Registry is about 70%, and thus, the conclusion limited. In our series, only 2.8% of patients had grade 2 autograft valve regurgitation, and no grade 3 or 4 regurgitation was identified, reflecting 93.6% completeness of follow-up.

Our data also demonstrated that the Ross procedure permitted recovery of left ventricular function, particularly when it had been altered by a long-standing aortic regurgitation. The present study demonstrated that this benefit persists over time: LVTD (55.5 ± 9.1 mm versus 51.8 ± 7.5 mm, p < 0.001) and LV index mass (150.7 ± 52.6 g/m2 versus 108.5 ± 32.3 g/m2, p < 0.001) significantly decreased, and left ventricular ejection fraction (0.646 ± 0.101 versus 0.681 ± 0.094%, p = 0.007) increased during follow-up. Our results are thus in agreement with those of Moidl and colleagues [6], who demonstrated that the Ross procedure results in more complete and more rapid return of left ventricular function and volumes than with other substitutes.

In conclusion, our current experience with the Ross procedure suggests that replacement of the aortic root by a pulmonary autograft can be safely performed in infants, children, and adults and is associated with low mortality and morbidity rates. So far, inappropriate enlargement of the autograft has not been observed in adults. The Ross procedure does not require permanent anticoagulation and is associated with low rates of endocarditis, thromboembolism, and degeneration. It constitutes an elegant alternative to the use of prosthetic valves in the treatment of aortic valve diseases.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Ross DN. Replacement of aortic and mitral valves with a pulmonary autograft Lancet 1967;2:956-958.[Medline]
  2. Ross DN, Jackson M, Davies J. The pulmonary autograft—a permanent aortic valve Eur J Cardiothorac Surg 1992;6:113-117.[Abstract]
  3. Elkins RC. The Ross operation: applications to children Semin Thorac Cardiovasc Surg 1996;8:345-349.[Medline]
  4. Kouchoukos NT, Davila-Roman VG, Spray TL, Murphy SF, Perrillo JB. 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]
  5. Simon P, Aschauer C, Moidl R, et al. Growth of the pulmonary autograft after the Ross operation in childhood Eur J Cardiothorac Surg 2001;19:118-121.[Abstract/Free Full Text]
  6. Moidl R, Simon P, Aschauer C, et al. Does the Ross operation fulfil the objective performance criteria established for new prosthetic heart valves? J Heart Valve Dis 2000;9:190-194.[Medline]
  7. Schoof PH, Hazekamp MG, van Wermeskerken GK, et al. Disproportionate enlargement of the pulmonary autograft in the aortic position in the growing pig J Thorac Cardiovasc Surg 1998;115:1264-1272.[Abstract/Free Full Text]
  8. Chambers JC, Somerville J, Stone S, Ross DN. Pulmonary autograft procedure for aortic valve diseaseLong-term results of the pioneer series. Circulation 1997;96:2206-2214.[Abstract/Free Full Text]
  9. Elkins RC, Lane MM, McCue C. Pulmonary autograft reoperation: incidence and management Ann Thorac Surg 1996;62:450-455.[Abstract/Free Full Text]
  10. David TE, Omran A, Ivanov J, et al. Dilation of the pulmonary autograft after the Ross procedure J Thorac Cardiovasc Surg 2000;119:210-220.[Abstract/Free Full Text]
  11. Takkenberg JJM, Dossche KME, Hazekamp MG, et al. Dutch Ross Study Group Report of the Dutch experience with the Ross procedure in 343 patients Eur J Cardiothorac Surg 2002;22:70-77.[Abstract/Free Full Text]
  12. Takkenberg JJM, Zondervan PE, van Herwerden LA. Progressive pulmonary autograft root dilatation and failure after Ross procedure Ann Thorac Surg 1999;67:551-554.[Abstract/Free Full Text]
  13. Sundt TM, Moon MR, Xu H. Reoperation for dilatation of the pulmonary autograft after the Ross procedure J Thorac Cardiovasc Surg 2001;122:1249-1252.[Free Full Text]
  14. Ley RG, Kofidis T, Fischer S, Kallenbach K, Harringer W, Haverich A. Aortic root reimplantation for successful repair of insufficient pulmonary autograft valve after the Ross procedure J Thorac Cardiovasc Surg 2002;124:1048-1049.[Free Full Text]
  15. Sievers HH, Leyh R, Loose R, Guha M, Petry A, Bernhard A. Time course of dimension and function of the autologous pulmonary root in the aortic position J Thorac Cardiovasc Surg 1993;105:775-780.[Abstract]
  16. Hokken RB, Bogers AJJ, Taams MA, et al. Does the pulmonary autograft in the aortic position in adults increase in diameter?An echocardiographic study. J Thorac Cardiovasc Surg 1997;113:667-674.[Abstract/Free Full Text]
  17. Carr-White GS, Afoke A, Birks EJ, et al. Aortic root characteristics of human pulmonary autografts Circulation 2000;102(suppl III):III-15-III-21.[Medline]
  18. Simon-Kupilik N, Bialy J, Moidl R, et al. Dilatation of the pulmonary autograft root after the Ross operation Eur J Cardiothorac Surg 2002;21:470-473.[Abstract/Free Full Text]
  19. Perry GJ, Helmoke F, Nanda NC, Byard C, Soto B. Evaluation of aortic insufficiency by Doppler color flow mapping J Am Coll Cardiol 1987;9:952-959.[Abstract]
  20. Baudet EM, Puel V, McBride JT, et al. Long-term results of valve replacement with the St. Jude medical prosthesis J Thorac Cardiovasc Surg 1995;109:858-870.[Abstract]
  21. Laske A, Jenni R, Maloigne M, Vassali G, Bertel O, Turina M. Pressure gradients across bileaflet aortic valve by direct measurement and echocardiography Ann Thorac Surg 1996;10:1097-1106.
  22. Jaffe WM, Coverdale HA, Roche AHG, Whitlock RML, Barratt-Boyes BG. Rest and exercise hemodynamics of 20–23 mm allograft, Medtronic intact (porcine) and St-Jude Medical valves in aortic position J Thorac Cardiovasc Surg 1990;100:167-174.[Abstract]
  23. Sanders SP, Levy RJ, Freed, MD, Norwood WI, Castaneda AR. Use of Hancock porcine xenografts in children and adolescents Am J Cardiol 1980;46:429-438.[Medline]
  24. Elkins RC, Santangelo K, Randolph JD, et al. Pulmonary autograft replacement in childrenThe ideal solution?. Ann Surg 1992;216:363-371.[Medline]
  25. Hokken RB, Bogers AJ, Taams MA, et al. Aortic root replacement with a pulmonary autograft Eur J Cardiothorac Surg 1995;9:378-383.[Abstract]
  26. Elkins RC, Knott-Craig CJ, Ward KE, Lane MM. The Ross operation in children: 10-year experience Ann Thorac Surg 1998;65:496-502.[Abstract/Free Full Text]
  27. Oury JH, Hiro SP, Maxwell JM, Lamberti JJ, Duran CM. The Ross procedure: current registry results Ann Thorac Surg 1998;66(suppl):S162-S165.[Medline]
  28. Elkins RC, Lane MM, McCue C, Ward KE. Pulmonary autograft root replacement: mid-term results J Heart Valve Dis 1999;8:499-506.[Medline]
  29. Daenen WA, Jalalia H, Eyskensb B, Gewilligb M. Mid-term results of the Ross procedure Eur J Cardiothorac Surg 1998;6:673-677.
  30. Elkins RC, Knott-Craig CJ, Howell CE. Pulmonary autografts in patients with aortic annulus dysplasia Ann Thorac Surg 1996;61:1141-1145.[Abstract/Free Full Text]
  31. Jenkins KJ, Hanley FL, Colan SD, Mayer Jr JE, Castaneda AR, Wernovsky G. Function of the pulmonary valve in the systemic circulation Circulation 1991;84(suppl III):III-173-III-179.[Medline]
  32. Allen MD, Shoji Y, Fujimura Y, et al. Growth and cell viability of aortic versus pulmonic homografts in the systemic circulation Circulation 1991;84(suppl III):III-94-III-99.[Medline]
  33. Elkins RC. The Ross operation: a 12-year experience Ann Thorac Surg 1999;68:S14-S18.[Medline]
  34. Tantengco VT, Humes RA, Clapp SK, et al. Aortic root dilation after Ross procedure Am J Cardiol 1999;83:6915–20.[Medline]
  35. Sonnenberg BH, Woo A, Omran AS, et al. Mid-term clinical and echocardiographic follow-up after Ross procedure J Am Coll Cardiol 1999;33(suppl):554A.
  36. Savoye C, Auffray JL, Hubert E, et al. Echocardiographic follow-up after Ross procedure in 100 patients Am J Cardiol 2000;85:854-857.[Medline]



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