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Ann Thorac Surg 2009;88:609-615. doi:10.1016/j.athoracsur.2009.04.100
© 2009 The Society of Thoracic Surgeons
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Original Articles: Pediatric Cardiac

Homograft Performance in Children After the Ross Operation

Jürgen Hörer, MD, PhDa,f,*,*, Thorsten Hanke, MDb,f,*, Ulrich Stierle, MDb,f, Johanna J.M. Takkenberg, MD, PhDc,f, Ad J.J.C. Bogers, MD, PhDc,f, Wolfgang Hemmer, MDd,f, Joachim G. Rein, MDd,f, Roland Hetzer, MD, PhDe,f, Michael Hübler, MDe,f, Derek R. Robinson, MS, DPhile,f, Hans H. Sievers, MDb,f, Rüdiger Lange, MD, PhDa,f

a Department of Cardiovascular Surgery, German Heart Center Munich at the Technical University, Munich, Germany
b Department of Cardiac Surgery, University Clinic Schleswig-Holstein, Campus Luebeck, Luebeck, Germany
c Department of Cardiothoracic Surgery, Erasmus University Medical Center, Rotterdam, the Netherlands
d Sana Herzchirurgische Klinik, Stuttgart, Germany
e German Heart Center, Berlin, Germany
f Department of Mathematics, School of Science and Technology, University of Sussex, Brighton, United Kingdom

Accepted for publication April 24, 2009.

* Address correspondence to Dr Hörer, Department of Cardiovascular Surgery, German Heart Center Munich at the Technical University, Lazarettstrasse 36, Munich, D-80636, Germany (Email: hoerer{at}dhm.mhn.de).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Background: The Ross operation may be the ideal aortic valve replacement in pediatric patients. However, reoperations for replacement of the homograft in the pulmonary position are inevitable. This study determined influencing factors for the development of homograft stenosis and regurgitation in pediatric Ross patients.

Methods: Follow-up echocardiograms of 116 children (86 boys) undergoing Ross operations at a mean age, 9.3 ± 4.9 years were analyzed using hierarchic multilevel modeling. Mean duration of the echocardiographic follow-up was 5.3 ± 4.2 years (609 patient-years, 398 examinations).

Results: Median homograft diameter z value was 0.3 (range –2.2 to +7.3). Mean homograft pressure gradient at implantation was 5.0 mm Hg with a significant increase of 4.2 mm Hg/y (p < 0.001) within the first 2 years and a steady state thereafter. Older donor age was significantly associated with lower mean pressure gradient at implantation (p = 0.037). Larger z value had no significant influence on the annual increase of pressure gradient (p = 0.87). Mean grade of regurgitation at implantation was 0.9, without significant annual increase (0.02 grade/y, (p = = 0.32). Older recipient (p = 0.005) and donor age (p < 0.0001) were significantly associated with lower mean regurgitation at implantation. Larger z value was associated with a higher annual increase of regurgitation (p = 0.014).

Conclusions: Relevant midterm homograft regurgitation is rare in children after the Ross operation. However, a significant annual increase occurs in the pressure gradient that cannot be influenced by larger graft size. Homograft oversizing may lead to a higher annual increase of regurgitation.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Homograft reconstruction of the right ventricular outflow tract has become a classic surgical approach as a part of total correction of numerous congenital heart lesions. This technique has made possible successful repair of pulmonary atresia with ventricular septal defect, complex forms of tetralogy of Fallot, common arterial trunk, transposition of the great arteries with pulmonary stenosis, and other forms of complex congenital heart disease [1–3]. Homograft reconstruction of the right ventricular outflow tract it is also performed during the Ross operation [4].

Most of these operations are performed in infancy; hence, implantation of large conduits was recommended because of the lack of growth potential of the cryopreserved valve [5–7]. This was supported by studies that reported smaller conduit size and younger patient age at the time of implantation to be significant risk factors for homograft failure [2, 8–10]. However, there is also evidence that conduit size is not the main determinant of homograft failure. Other factors, such as pulmonary or aortic origin, type of preservation, recipient and donor gender and AB0 group, implantation site, and the underlying heart defect may influence homograft degeneration before somatic outgrowth [2, 10–14].

The goal of the present study was to identify determinants for the development of homograft gradient and regurgitation in a homogenous population of children aged younger than 16 years who had undergone Ross operations and were at high-risk for somatic outgrowth.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Institutional Review Board approval was obtained to conduct this prospective follow-up study. The requirement for patients to provide their informed consent was waived.

Study Population and Operative Data
Data from the Dutch-German Ross Registry database were analyzed. The study included 116 patients from four departments of cardiac surgery in Germany and one in the Netherlands. The patients were younger than 16 years old at the time of the Ross operation and received a homograft in the pulmonary position (Figs 1 and 2). Go The Ross operations were performed between September 1999 and July 2005. The initial and follow-up data from each center were collected retrospectively for the time before 2002, and prospectively thereafter.


Figure 1
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  		Fig 1. Age distribution of children at the time of the Ross operation.

 

Figure 2
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  		Fig 2. Distribution of the diameters (in mm) of the implanted homografts.

 
The surgical technique was determined by the responsible surgeon at each center. Patient characteristics are listed in Table 1. Details of the operative techniques have been described elsewhere [15–17]. The homografts were provided by the surgical departments or purchased from different companies. The procurement of raw material, processing, and preservation was performed according to center-specific protocols or according to the manufacturers' notes.


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  		Table 1 Patient Characteristics
 
Clinical Follow-Up
Follow-up investigations were routinely scheduled at discharge and annually thereafter. The measurements of dimensions were accomplished by experienced pediatric sonographers at each center. Because it was a multicenter study, the final decision of regurgitation grading was left to the decision of the echocardiographer's preference and experience at each center. Patients underwent a mean of 3.4 ± 2.5 echocardiographic examinations (range, 1 to 13). Mean duration of the echocardiographic follow-up was 5.3 ± 4.2 years (609 patient-years, 398 examinations). Annual echocardiographic data were available for 54 patients (46.6%), 30 (25.9%) underwent echocardiographic examinations at least every 2 years, and the intervals between examinations for 32 patients (27.6%) were more than 2 years.

Echocardiographic Data Acquisition and Measurements
All measurements were performed with the inner edge to inner edge technique. Measurements of dimensions were made perpendicular to the parasternal long axis view at end diastole. The z values of homograft diameters were estimated according to the nomograms published by Daubeney and colleagues [18] on the basis of the body surface area (BSA) and the echocardiographically derived measurement.

Homograft regurgitation was graded by mapping the dimensions of the regurgitation jet with pulsed and color flow Doppler echocardiography [19]. The width of the proximal pulmonary regurgitation jet and the density and deceleration rate of the spectral Doppler flow signal were included in the assessment of regurgitation severity. This was graded from 0 to 4 (0 = none, 1 = mild, 2 = moderate, 3 = moderately-severe, 4 = severe). Trace (trivial) insufficiency, defined as a very tiny regurgitation jet in early diastole near the detection limit, was included in the analyses as grade 0.5.

Maximum velocities across the pulmonary homograft were obtained by continuous Doppler interrogation of the basal short axis. Pressure gradients across the right ventricular outflow tract were calculated by the modified Bernoulli equation. The mean pressure gradients were used for all analyses.

Statistical Analysis
Frequencies are given as absolute numbers and percentages. Continuous data are expressed as means with standard deviation or median with ranges. Statistical analysis of clinical variables and initial fitting was performed using SPSS 16.0 software (SPSS Inc, Chicago, IL).

To perform appropriate longitudinal analysis of homograft valve function over time as proposed by the guidelines of reporting death and morbidity after cardiac valve interventions [20], the echocardiographic data were analyzed by using the multilevel hierarchical linear model (MLwiN 2.0, Centre for Multilevel Modeling, London, United Kingdom). This model provides a linear regression line with an intercept (± standard error) and slope (± standard error) for each patient. The intercept corresponds to the initial value at the end of the operation, and the slope represents the annual progression of these measures.

The best fitting model to study the development of the mean gradient with time was a change-point model with a linear increase of the homograft mean gradient until 2 years and flattening out in a steady state afterwards. Because the development of homograft regurgitation was smoothly gradual for the time frame studied, a linear increase with time was assumed. The covariables studied were patient and donor age, patient and donor gender, and homograft diameter z value.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Footnotes
 Acknowledgments
 References
 
Homograft Gradient
Within the first 2 postoperative years, the term to estimate changes in mean homograft pressure gradient in the total study population was:


Formula 1

(1)

Hence, the initial gradient at the time of implantation was 4.97 mm Hg, with a significant annual increase of 4.15 mm Hg (p < 0.0001). From the third postoperative year onward, there is no more progression of the gradient, so that the homograft pressure gradient then equals the initial gradient plus twice the annual increase (Fig 3).


Figure 3
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  		Fig 3. Plot of estimates of the development of homograft gradients.

 
Influencing Factors for Homograft Gradient
The previously described model was extended to allow for both the intercept and slope to depend on the covariables. Accordingly, older donor age was significantly associated with lower mean pressure gradient at implantation (p = 0.037, Fig 4A). Recipient age at the time of operation (Fig 4B) and homograft diameter z value had neither significant influence on the initial gradient nor on the annual increase of the gradient (Fig 4C). The initial gradient did not vary significantly depending on recipient or donor gender. The annual increase of the gradient did not vary significantly depending on donor age or recipient or donor gender (Table 2).


Figure 4
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  		Fig 4. Plot of estimates of the development of homograft gradients calculated for (A) different donor ages, (B) recipient age groups, and (C) different z values of the homografts.

 

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  		Table 2 Significance of Potential Influencing Factors for the Initial Homograft Gradient and the Development of Homograft Gradient Over Time
 
Homograft Regurgitation
The best fitting model to study regurgitation was a linear model with the term:


Formula 2

(2)

Hence, the initial grade of homograft regurgitation at the time of implantation was 0.89 with an annual increase of 0.02. The initial regurgitation was significantly non-zero (p < 0.0001); however, there was no significant evidence for an increase in homograft regurgitation over time (p = 0.32, Fig 5).


Figure 5
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  		Fig 5. Plot of estimates of the development of homograft regurgitation.

 
Influencing Factors for Homograft Regurgitation
The above model was extended to allow for both the intercept and slope to depend on the covariables. Accordingly, older donor age was significantly associated with lower mean regurgitation at implantation (p < 0.0001, Fig 6A). The initial regurgitation was significantly higher in patients who were younger at the time of implantation (p = 0.005, Fig 6B). The initial regurgitation did not vary significantly depending on homograft diameter z value or recipient or donor gender. The increase of regurgitation was significantly higher in patients who received larger homografts according to z values (p = 0.014, Fig 6C). The increase of regurgitation did not vary significantly depending on recipient or donor age, or recipient or donor gender (Table 3).


Figure 6
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  		Fig 6. Plot of estimates of the development of homograft regurgitation calculated for (A) different donor ages, (B) recipient age groups, and (C) different z values of the homografts.

 

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  		Table 3 Significance of Potential Influencing Factors for the Initial Homograft Regurgitation and the Development of Homograft Regurgitation Over Time
 
Reoperations and Reinterventions
During follow-up, 13 patients required 21 homograft reoperations or reintervention. Six patients had one reoperation, 1 patient had two reoperations, and 1 patient had three reoperations for homograft exchange. Two patients underwent one balloon valvulotomy, each. Two patients underwent two interventions each before homograft exchange, and 1 patient underwent balloon valvulotomy after homograft exchange. The indication for homograft reintervention or exchange was predominant stenosis in all patients. Freedom from homograft reoperation or reintervention was 91.0% ± 2.9% at 5 years and 80.6% ± 6.5% at 10 years. Only echocardiographic measurements before the first homograft reintervention or reoperation were included into the multilevel analysis of gradient and regurgitation.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Footnotes
 Acknowledgments
 References
 
In the present study group, we observed a significant development of homograft stenosis within the first 2 years. Freedom from homograft reoperation or reintervention was 80.6% ± 6.5% at 10 years. The indication for homograft reintervention or exchange was predominant stenosis in all patients. The development of regurgitation was not of great importance.

The development of homograft stenosis was not influenced by any of the studied variables. Especially, the increase of the gradient was not significantly lower in homografts that were larger than the predicted pulmonary annulus according to the patients' BSA. This contrasts with the results of some authors who suggest the use of oversized homografts to compensate for somatic growth [5–7, 14].

The data presented by Karamlou and colleagues [21] support our results. They found no significant difference in freedom from reoperations in patients who received a homograft with a diameter larger than one standard deviation of the predicted pulmonary annulus according to the patients' BSA compared with patients who received a smaller homograft. An explanation of our findings may be that the orifice area of an implanted oversized homograft might effectively not be larger compared with a homograft that was adjusted to the patient's BSA due to the lack of space and potential sternal compression. Wells and colleagues [13] even speculated that external compression might predispose the oversized homograft to early failure due to contracture and shrinkage. Hence, according to the present results, there is no advantage of larger grafts.

In addition, there may be a disadvantage of larger grafts. Homograft regurgitation developed significantly faster in patients who received larger homografts according to z values. Larger homografts showed higher grade of regurgitation after the second postoperative year. Within the first 2 years after implantation, an inverse relationship develops between homograft size and regurgitation. Larger homografts showed less regurgitation at the time of implantation. The cause for this observation might be the effect of external compression of an oversized homograft. This may lead to flattening and geometric distortion of the cusps. Initially, there may be no regurgitation due to excessive cusp material; however, there might be a fast development of regurgitation as a consequence of accelerated degeneration processes.

The statistical method in the present analysis does not provide a cutoff value for the size of homografts. However, we discourage the use of homografts with z values larger than 3 because the development of the gradient is not slower compared with smaller grafts and the expected regurgitation at 8 years is mild to moderate.

The development of regurgitation in the overall study population is not of great importance, and the mean regurgitation 8 years after implantation is estimated to be mild. In contrast, Basket and colleagues [14] observed more than moderate regurgitation in 15 of 38 patients within 5 years after homograft implantation. This difference may be explained by the more favorable homograft performance in Ross patients [22–24], considering that the cohort studied by Basket and colleagues consisted exclusively of non-Ross patients. Boethig and colleagues [25] reported that 30% of Ross patients and 70% of non-Ross patients presented with at least moderate regurgitation 10 years after the initial implantation.

In the present study, younger donor age was predictive for both higher initial regurgitation and higher initial gradient. We have no explanation for this finding. Baskett and colleagues [14] showed that shorter retrieval-to-preservation time correlates with homograft failure. Hence, a main influencing factor for early homograft failure may be the preserved cell viability of the cryopreserved homograft valve [23]. Owing to the character of multicenter studies, and therefore the various origins of the implanted homografts, the effect of different harvesting protocols and preservation types could not be analyzed.

In summary, substantial development of homograft gradient occurs within the first 2 years after implantation but not significant development of regurgitation over time. The development of gradient is not slower in larger homografts, but the development of regurgitation is faster. Hence, we discourage the use of homografts with z values larger than 3. Homografts from older donors show lower gradient and lower regurgitation initially and during follow-up; therefore, the use of homografts from older donors should be considered.

The current study presents several limitations. A bias of the use of echocardiographic evaluations from different centers using different methods cannot be excluded and may have influenced the results. The presented results of homograft performance are limited to homografts that were placed orthotopically during a Ross operation. Because homograft performance is unfavorable in non-Ross patients [22], the present data and conclusions cannot be transferred to the behavior of homografts in general. In addition, the study included a small subgroup with the use of an aortic homograft that was too small for subgroup analysis of key items.

Finally, a main limitation of the study is the evolution of the surgical approach within the last 15 years. Changes in preoperative, operative, and postoperative management may have affected the outcome parameters in a way not covered by our analysis.

However, the present analysis has several advantages compared with previous reports on homograft performance. Because the development of gradient and regurgitation is a process that evolves with time, the study of repeated longitudinal echo data in the present analysis may be more appropriate to describe homograft performance compared with the analysis of actuarial estimates of freedom from events [20, 25]. The present study only included children aged younger than 16 years at the time of the homograft implantation. Hence, the effect of potential risk factors could be studied in a cohort at high-risk for somatic outgrowth.

Finally, the study focused on a homogenous cohort that underwent Ross operations. Therefore, the development of gradient and regurgitation could be studied as a function of donor-specific potential risk factors in the absence of previously described recipient-specific risk factors such as the underlying heart defect [22, 24].


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
References
 
We thank Katrin Meyer for her excellent data management and secretarial support at the Registry Site at the Department of Cardiac Surgery, University Hospital Schleswig-Holstein, Campus Lübeck.


   Footnotes
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
Acknowledgments
 References
 
* Both authors contributed equally to the study. Back


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 

  1. Ross DN, Somerville J. Correction of pulmonary atresia with a homograft aortic valve Lancet 1966;2:1446-1447.[Medline]
  2. Dearani JA, Danielson GK, Puga FJ, et al. Late follow-up of 1095 patients undergoing operation for complex congenital heart disease utilizing pulmonary ventricle to pulmonary artery conduits Ann Thorac Surg 2003;75:399-410discussion 410–1.[Abstract/Free Full Text]
  3. Lange R, Weipert J, Homann M, et al. Performance of allografts and xenografts for right ventricular outflow tract reconstruction Ann Thorac Surg 2001;71:S365-S367.[Medline]
  4. Ross DN. Replacement of aortic and mitral valves with a pulmonary autograft Lancet 1967;2:956-958.[Medline]
  5. Perron J, Moran AM, Gauvreau K, del Nido PJ, Mayer Jr JE, Jonas RA. Valved homograft conduit repair of the right heart in early infancy Ann Thorac Surg 1999;68:542-548.[Abstract/Free Full Text]
  6. Forbess JM, Shah AS, St Louis JD, Jaggers JJ, Ungerleider RM. Cryopreserved homografts in the pulmonary position: determinants of durability Ann Thorac Surg 2001;71:54-59discussion 59–60.[Abstract/Free Full Text]
  7. Tam RK, Tolan MJ, Zamvar VY, et al. Use of larger sized aortic homograft conduits in right ventricular outflow tract reconstruction J Heart Valve Dis 1995;4:660-664.[Medline]
  8. Caldarone CA, McCrindle BW, Van Arsdell GS, et al. Independent factors associated with longevity of prosthetic pulmonary valves and valved conduits J Thorac Cardiovasc Surg 2000;120:1022-1030discussion 1031.[Abstract/Free Full Text]
  9. Clarke DR, Bishop DA. Allograft degeneration in infant pulmonary valve allograft recipients Eur J Cardiothorac Surg 1993;7:365-370.[Abstract/Free Full Text]
  10. Meyns B, Jashari R, Gewillig M, et al. Factors influencing the survival of cryopreserved homografts. The second homograft performs as well as the first. Eur J Cardiothorac Surg 2005;28:211-216discussion 216.[Abstract/Free Full Text]
  11. Javadpour H, Veerasingam D, Wood AE. Calcification of homograft valves in the pulmonary circulation–is it device or donation related? Eur J Cardiothorac Surg 2002;22:78-81.[Abstract/Free Full Text]
  12. Heinemann MK, Hanley FL, Fenton KN, Jonas RA, Mayer JE, Castaneda AR. Fate of small homograft conduits after early repair of truncus arteriosus Ann Thorac Surg 1993;55:1409-1411discussion 1411–2.[Abstract/Free Full Text]
  13. Wells WJ, Arroyo Jr H, Bremner RM, Wood J, Starnes VA. Homograft conduit failure in infants is not due to somatic outgrowth J Thorac Cardiovasc Surg 2002;124:88-96.[Abstract/Free Full Text]
  14. Baskett RJ, Nanton MA, Warren AE, Ross DB. Human leukocyte antigen-DR and ABO mismatch are associated with accelerated homograft valve failure in children: implications for therapeutic interventions J Thorac Cardiovasc Surg 2003;126:232-239.[Abstract/Free Full Text]
  15. Sievers HH, Hanke T, Stierle U, et al. A critical reappraisal of the Ross operation: renaissance of the subcoronary implantation technique? Circulation 2006;114:I504-I511.[Medline]
  16. Duebener LF, Stierle U, Erasmi A, et al. Ross procedure and left ventricular mass regression Circulation 2005;112:I415-I422.[Medline]
  17. Bohm JO, Botha CA, Rein JG, Roser D. Technical evolution of the Ross operation: midterm results in 186 patients Ann Thorac Surg 2001;71:S340-S343.[Medline]
  18. Daubeney PE, Blackstone EH, Weintraub RG, Slavik Z, Scanlon J, Webber SA. Relationship of the dimension of cardiac structures to body size: an echocardiographic study in normal infants and children Cardiol Young 1999;9:402-410.[Medline]
  19. Perry GJ, Helmcke 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. Akins CW, Miller DC, Turina MI, et al. Guidelines for reporting mortality and morbidity after cardiac valve interventions Ann Thorac Surg 2008;85:1490-1495.[Free Full Text]
  21. Karamlou T, Ungerleider RM, Alsoufi B, et al. Oversizing pulmonary homograft conduits does not significantly decrease allograft failure in children Eur J Cardiothorac Surg 2005;27:548-553.[Abstract/Free Full Text]
  22. Brown JW, Ruzmetov M, Rodefeld, MD, Vijay P, Turrentine MW. Right ventricular outflow tract reconstruction with an allograft conduit in non-ross patients: risk factors for allograft dysfunction and failure Ann Thorac Surg 2005;80:655-663discussion 663–4.[Abstract/Free Full Text]
  23. Niwaya K, Knott-Craig CJ, Lane MM, Chandrasekaren K, Overholt ED, Elkins RC. Cryopreserved homograft valves in the pulmonary position: risk analysis for intermediate-term failure J Thorac Cardiovasc Surg 1999;117:141-146; discussion 46–7.[Abstract/Free Full Text]
  24. Jashari R, Daenen W, Meyns B, Vanderkelen A. Is ABO group incompatibility really the reason of accelerated failure of cryopreserved allografts in very young patients?–Echography assessment of the European Homograft Bank (EHB) cryopreserved allografts used for reconstruction of the right ventricular outflow tract Cell Tissue Bank 2004;5:253-259.[Medline]
  25. Boethig D, Goerler H, Westhoff-Bleck M, et al. Evaluation of 188 consecutive homografts implanted in pulmonary position after 20 years Eur J Cardiothorac Surg 2007;32:133-142.[Abstract/Free Full Text]



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