Ann Thorac Surg 2007;83:1774-1780
© 2007 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Geometric Disproportion of Cardiac Structure and Graft Ischemia Affect Tricuspid Valve Regurgitation Early After Neonatal Heart Transplantation
Miki Asano, MD, PhD,
Anees J. Razzouk, MD,
Richard E. Chinnock, MD,
Leonard L. Bailey, MD*
Departments of Surgery and Pediatrics, Cardiology, Loma Linda University School of Medicine and Medical Center, Loma Linda, California
Accepted for publication December 19, 2006.
* Address correspondence to Dr Bailey, Departments of Surgery and Pediatrics, Cardiology, Loma Linda University School of Medicine and Medical Center, 11175 Campus St, Room 21120, Loma Linda, CA 92354 (Email: lbailey{at}som.llu.edu).
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Abstract
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Background: Although tricuspid valve regurgitation (TR) after heart transplantation is a known complication, there has been little discussion of this subject in neonatal heart transplantation. We aim to elucidate the prevalence, etiology, and evolution of TR early after transplant in neonates.
Methods: Eighty-five neonatal recipients were studied retrospectively by two-dimensional and Doppler echocardiography. The semiquantitative grading of TR was based on the ratio of regurgitation jet area to right atrial area.
Results: Immediately after neonatal heart transplantation, TR was recognized in 47 patients (grade 1, n = 18; grade 2, n = 22; grade 3, n = 7; and grade 4, n = 0). Tricuspid regurgitation prevalence diminished from 55% to 19% with reduction in severity 1 year after transplantation. The prevalence of TR (grade 2 and grade 3) was affected by a donor/recipient body weight ratio of more than 2.0 (p = 0.004) and graft ischemia for more than 3 hours (p = 0.014). The ratio of donor and recipient right atria portion, which had a correlation with donor/recipient body weight ratio (r2 = 0.415, p < 0.0001), separated the four subgroups in terms of TR grade immediately after transplantation (p = 0.0064) and also at 1 year after transplantation in all surviving grafts from 1.48 ± 0.54 to 0.8 ± 0.32 (p < 0.0001). The Cox model found no significance for early posttransplant TR as a risk factor for graft survival.
Conclusions: Early posttransplant TR was affected by atria geometrical disproportion and by graft ischemia. Tricuspid regurgitation was not a risk factor for graft survival because of its amelioration over time, perhaps induced by recipient growth and recovery of myocardial injury relating to graft procurement.
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Introduction
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Tricuspid valve regurgitation (TR) is frequently observed after orthotopic heart transplantation in adults, with a prevalence of 84% to 97% [1–3]. Some have reported that both prevalence and severity increase during the follow-up period [4]. Although the etiology and the significance of TR among adult recipients is debated, there has been little mention of this issue as it pertains to children, especially the neonatal recipient, whose heart graft tricuspid valve could be challenged unpredictably by intermittent changes in pulmonary vascular resistance. This retrospective study aims to elucidate the incidence, etiology, and evolution of early TR after neonatal heart transplantation.
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Patients and Methods
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Patients
We studied 87 consecutive neonates (less than 30.4 days after birth) from among 334 pediatric recipients who underwent orthotopic heart transplantation between May 1988 and January 2000 at Loma Linda University Medical Center and Children’s Hospital, California, using two-dimensional and Doppler echocardiography. Two recipients who received grafts with mild atrioventricular valve regurgitation were excluded. Of these 85 recipients, 53 were male and 32 were female, and the mean age was 17.3 ± 7.4 days (range, 0.2 to 29). Preoerative diagnosis was hypoplastic left heart syndrome in 63 patients, other congenital heart disease in 21 patients (common atrioventricular canal in 5, single left ventricule in 3, Shone’s complex in 3, aortic arch interruption in 3, pure pulmonary atresia in 2, tetralogy of Fallot with pulmonary atresia in 2, aortic stenosis in 1, truncus arteriosus in 1, and Ebstein’s anomaly in 1), and dilated cardiomyopathy in 1. Follow-up was completed to January 2002, or at the time of initial graft loss. Mean follow-up was 86.1 ± 46.9 months, ranging from 12.5 to 154.8 months. This retrospective study was conducted in accordance with the guidelines formulated by the Institutional Review Board, with the waiver of need for patient consent as verified by the Board’s chairman subsequently.
Procedures and Immunosuppression Therapy
Neonatal heart transplantation was performed with technical maneuvers described previously [5–7]. In brief, a median sternotomy was utilized to perform thymectomy and expose the recipient’s native heart. If the donor heart was significantly larger than the native heart, the entire left pericardium anterior to the phrenic nerve was removed. Single venous and arterial cannulation was generally employed for cardiopulmonary bypass. Cardiectomy was performed, leaving behind right and left atrial cuffs. The donor graft was anastomosed to the recipient atrial cuff with a continuous polypropylene suture (7-0), starting at the lowest portion of the interatrial septum and then proceeding to complete the right atrial anastomosis first. The graft was reflected toward the operating surgeon, and the left atrial anastomosis was completed. Aortic arch reconstruction (as needed) and pulmonary artery anastomosis completed the implantation.
Standard maintenance antirejection therapy consisted of cyclosporine (10 to 20 mg/kg daily) and azathioprine (1 to 3 mg/kg daily, keeping the white blood cell count more than 4,000/mL). Immunosuppression therapy was maintained at higher levels for those who had had a difficult rejection course, including long-term methotrexate in place of azathioprine. As rescue therapy for acute cellular rejection, methylprednisolone (20 to 25 mg/kg intravenously every 12 hours for 8 doses), or methotraxate (10 mg/m2 per week administered as a single dose or as a three-dose regimen given every 12 hours once weekly or divided three times weekly) or antithymocyte globulin (15 mg/kg daily for 7 to 10 days), or both, was used.
Evaluation of TR and Intracardiac Dimensions of Graft
Two-dimensional and Doppler echocardiographic studies were performed in patients using a commercially available Hewlett-Packard echocardiograph (Sonos 1500, 5000; Hewlett-Packard Co, Palo Alto, CA). Studies were obtained within a week after transplantation, with regular follow-up examinations [8]. Images were recorded on videotape for off-line analysis. Tricuspid regurgitation was considered present if mosaic or blue signals originated from the atrial aspect of the valve during the systolic phase. Tricuspid regurgitation was mapped with color Doppler flow imaging by direct planimetry of the systolic regurgitant jet area. The ratio of regurgitant jet area to atrial area provided a semiquantitative assessment of regurgitation [9, 10]. In general, a regurgitant jet area to atrial area ratio of less than 10% was considered trivial (grade 1), 10% to 25% was mild (grade 2), 25% to 50% was moderate (grade 3), and greater than 50% was severe (grade 4).
Ventricular and valvular dimensional analyses were employed using electronic caliper measurements of frozen end-diastolic and end-systolic frames. Right ventricular diameters and lengths were measured as previously described [11, 12]. Annular diameters were measured in both the two-chamber and four-chamber views at the hinge points of the leaflets with the annulus [13]. The percentage of systolic shortening of the tricuspid valve annulus was assessed to evaluate the degree of sphincter effect [14]. Atrial areas, comprising both donor and recipient atrial portions, were planimetered in the four-chamber long axis view at systole, and provided an "hourglass" or "snowman" configuration of the atria created by the atrial anastomoses protruding into the atrial cavity (Fig 1). The ratio of the donor and recipient right atrial portions (D/R RA) was also determined [3]. To examine annuloventricular relations without reference to donor body size, the ratio of tricuspid systolic valve annular diameter to right ventricular length and the ratio of systolic annular diameter to ventricular diameter were calculated. Every echocardiographic assessment utilized in this study was performed in the absence of graft rejection and systemic infection.
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Fig 1. The four-chamber long-axis view provided an "hourglass" or a "snowman" configuration of the atria (dotted lines) by anastomoses protruding into the atrial cavity (arrow at asterisk).
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Definition of Rejection, Infection, Donor Down Time, and Pulmonary Hypertension
Rejection episodes were diagnosed and treated with rescue therapy based mainly on clinical symptoms and echocardiography [8]. We have typically not employed routine endomyocardial biopsies of neonate recipients to establish the diagnosis of rejection, defined as 3A or greater according to the criteria of the International Society of Heart and Lung Transplantation [15]. If more evidence would be needed for the diagnosis, however, endomyocardial biopsies were done. Infection episodes were defined by the need for intravenous antimicrobial therapy. Rejection and infection rate represent the number of treated acute rejections and infections during the initial graft surviving period divided by the number of months of that period. Donor down time meant the duration of donor cardiopulmonary resuscitation requiring cardiac massage and epinephrine injections before stabilization and the determination of brain death. Pulmonary hypertension was defined as a ratio of pulmonary artery pressure to systemic artery pressure at systole of more than 0.75 or mean pulmonary artery pressure more than 25 mm Hg, or both, evaluated by cardiac catheterization or echocardiography.
Statistical Analysis
All results are presented as mean ± SD. A Wilcoxon’s signed rank test and a Kruskal-Wallis test were used to compare paired and unpaired continuous variables of cardiac geometry and function among the groups of TR, respectively. Multiple logistic regression analyses were used for predicting risk factors of TR early after transplantation. Nominal variables in pulmonary hypertension recipients were compared by Fisher’s exact probability test. Correlation coefficients (r) and the linear regression equation between donor/recipient body weight ratio (D/R BW) and D/R RA were assessed by Spearman’s correlation. The Cox proportional hazards model was used for the univariate and multivariate prognostic risk analyses for immediate TR and other variables after transplantation. The receiver operating characteristics curve was used for sensitivity and specificity analysis for the variable of graft ischemia more than 3 hours in TR. The relative risk for occurrence of variables were calculated with 95% confidence intervals. All statistical analyses were performed by SPSS 12.0 J for Windows (SPSS, Chicago, Illinois). A p value of less than 0.05 was considered significant.
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Results
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Actuarial Graft Survival by Subgroups
Eleven grafts were lost because of acute rejection in 6 recipients, host infection in 3, and technical/management failure in 2 during 1 year after transplantation (Fig 2). In total, 19 grafts were eventually lost during the entire follow-up. The 1-, 5-, and 10-year actuarial graft survival rates of all recipients were 87%, 79%, and 75%, respectively. Among subgroups, there was no statistical significant difference in graft survival.
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Fig 2. Actuarial graft survival rate of subgroups. The 1-, 5-, and 10-year survival rates were 94%, 83%, and 83% among grade 1 tricuspid valve regurgitation (TR) recipients; and 82%, 77%, and 70% among grade 2 TR recipients, respectively. One grade 3 TR recipient died at 12 years after transplantation.
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Prevalence and Severity of TR Early After Neonatal Heart Transplantation
Tricuspid regurgitation was found in 47 of 85 recipients immediately after transplantation (55%), and the degree ranged from grade 1 to grade 3. Eighteen had grade 1 (21%), 22 had grade 2 (26%), and 7 grade 3 (8%; Fig 3). One year after transplantation, TR diminished in 14 of 74 recipients (19%) with a reduction of severity; that is, 9 had grade 1 (12%), 4 had grade 2 (6%), and 1 grade 3 (1%). At the end of the total follow-up period, TR existed in 15 of 66 recipients (23%), 9 with grade 1 (14%), 3 with grade 2 (4%), and 3 with grade 3 (4%).
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Fig 3. The prevalence and severity of tricuspid valve regurgitation after transplantation. (Open area = none; loosely dotted area = grade 1; closely dotted area = grade 2; hatched area = grade 3.)
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Potential Risk Factors for TR (Grade 2 and Grade 3) Early After Neonatal Heart Transplantation
The multiple logistic regression analysis found graft cold ischemic time (mean, 4.9 ± 1.9 hours; range, 1.1 to 9.6) of more than 3 hours to be an important risk factor for TR immediately after transplantation (Table 1). The variable of graft ischemia more than 3 hours showed that sensitivity and specificity were 92.7% and 39.1% in a receiver operating characteristics curve, respectively (Area Az = 0.653, p = 0.014, 95% confidence interval: 0.537 to 0.770). A D/R BW ratio more than 2.0 also increased the risk of TR by a factor of 4.6. Pulmonary hypertension showed the expected risk of TR by 0.9, without significance.
Comparison of Cardiac Geometry and Function Early After Transplantation Among the Groups
A remarkable difference existed in D/R RA among the groups (Table 2). Moreover, there was a significant correlation between D/R BW and D/R RA (Fig 4).
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Fig 4. Correlation between ratio of donor body weight to recipient body weight (D/R BW) and ratio of donor right atria to recipient right atria (D/R RA). A positive correlation existed with correlation coefficients of 0.453 (r2 = 0.415, p < 0.0001, 95% confidence interval: 0.5 to 0.75) by Spearman correlation.
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Recipients who had TR also had a reduced percentage of shortening of the valve annulus (p = 0.0447). Furthermore, recipients with greater TR had a statistically significant larger ratio of annular diameter to ventricular length, and also significant larger ratio of annular diameter to ventricular diameter.
Change of Geometric Variables Early After Transplantation Compared with 1 Year After Transplantation Among Surviving Grafts
The D/R RA was significantly reduced 1 year after transplantation from 1.48 ± 0.54 to 0.80 ± 0.32 among all surviving grafts (Table 3). Shortening of the tricuspid valve annulus increased remarkably from 14.7% ± 8.6% to 22.7% ± 12.1%. Tricuspid annular diameter/right ventricular length ratio decreased from 0.74 ± 0.25 to 0.53 ± 0.14 (p < 0.0001). Annular diameter/ventricular diameter ratio decreased but without significance. Right ventricular fractional shortening increased significantly, from 33.5% ± 15.5% to 39.9% ± 15.9%.
Prognostic Risk Analyses for Early TR and Other Variables
Using the Cox hazards model, TR early after neonatal heart transplantation was not a risk factor for graft survival (Table 4). Incidence of posttransplant coronary artery disease, increased rejection rate, and increased infection rate correlated with increased risk of graft loss.
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Table 4 Prognostic Risk Analyses for Early Tricuspid Valve Regugitation (TR) and Other Variables After Neonatal Heart Transplantation
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Comment
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The prevalence of TR early after transplantation was 55% in this study. By comparison, TR is detected in 8.5% of children with congenital heart disease and in 25% of newborns with respiratory distress. Only 3% to 6% of normal children exhibit significant TR [16, 17].
The etiology of early posttransplant TR in adult recipients has been discussed previously. These etiologies include acute allograft edema [18], papillary muscle dysfunction [19], remodeling of atrial size and geometry, cyclic torsion of the atria during ventricular systole and diastole, asynchronous contraction of the donor and recipient atrial compartment [20], and right ventricular enlargement caused by pulmonary hypertension [21–24].
It is possible that graft edema and papillary muscle dysfunction may result from graft ischemia during procurement and implantation [2]. In the present study, graft ischemic time of more than 3 hours was a potential risk factor for significant TR. Although no prolapsing of tricuspid valve leaflets was observed, shortening of the tricuspid valve annulus was remarkably reduced in significant TR recipients. The anatomic structures surrounding the annulus may influence the reduction in annular size. The mitral annulus has two major trigones; however, the tricuspid annulus has only a single fibrous trigone [3]. Therefore, the tricuspid annulus, with more of its circumference in contact with the myocardium, may be affected more easily in its sphincteric effect by myocardial ischemia. This idea is supported in that there have been no studies demonstrating a higher prevalence of mitral regurgitation among heart transplant recipients of any age [1–3, 18–20]. Among recipients in the present study, the prevalence of mitral valve regurgitation (39%) was lower than that of TR.
Size-mismatched grafts, with a D/R BW ratio greater than 2.0 and a corresponding increase in the D/R RA ratio, were an important pretransplant risk factor for immediate posttransplant TR. A prominent circular suture line separates donor and recipient atria, and creates a snowman-shaped atrium. Nonhomogeneous contraction of both atrial components may contribute to atrial dysfunction, reflected as TR. Traction placed on the tricuspid annulus by atrial free-wall donor-recipient suturing may contribute to early TR. One year after transplantation, a significant reduction of D/R RA ratio that accompanies recipient growth suggests improved atrial proportioning. This was characterized by decreasing incidence and severity of TR. Hence, growth might be an important factor in the amelioration of TR induced by a large donor/recipient size mismatch.
Before undergoing transplantation, the majority of adult recipients have some degree of pulmonary hypertension secondary to chronic elevation of left ventricular end-diastolic pressures. Exposure of the right ventricle to abnormal recipient pulmonary vascular resistance results in early posttransplant ventricular dilatation. This donor right ventricular remodeling results in TR that persists at 1-year follow-up despite resolution of pulmonary hypertension [24]. By contrast, pretransplant pulmonary hypertension in the neonate was not a risk factor for early TR.
In this study, most neonates who required heart transplantation had congenital anomalies in which the systemic circulation was ductus dependent or having left to right shunt by intracardiac lesion. Despite potentially huge left-to-right shunts, pulmonary vascular resistance in newborns is rarely fixed and usually falls significantly with the normalization of the pulmonary blood flow. Although the ventricles never seem to experience sustained increases in afterload or volume overload, we confirmed the right ventricular remodeling that occurs after neonatal heart transplantation in size-matched grafts [25]. Among oversized grafts, no significant change was observed in right ventricular volumes throughout the posttransplant period. There might be some degree of variable increase in afterload, such as pulmonary hypertension crisis and donor right ventricular dysfunction due to ischemia, which would stimulate right ventricular remodeling, whereas oversized grafts appeared to accommodate intermittent abnormal pulmonary vascular resistance without the necessity of hypertrophy or dilation, or both. Oversized grafts had both benefits and disadvantages. The influence of D/R BW on the incidence of TR was apparent, and perhaps owed more to geometry than to physiology.
The bicaval anastomosis technique should be free from distortion of geometry and asynchronous contraction resulting from the donor/recipient atrial connection [26, 27]. In neonates, there might be a higher risk of stenosis after bicaval direct anastomosis because of the absolute small size of recipient vena cava. Given the case of oversized graft, the distinct discrepancy of diameter of the vena cava between donor and recipient would strongly affect the occurrence of technical problem and of later stenosis. Unfavorable side effects would be possibly induced by this procedure [28]. Now that early posttransplant TR was confirmed by our study not to be a risk factor for graft survival because of its amelioration over time, little need of the bicaval anastomosis technique might exist in neonatal heart transplantation.
The clinical importance of TR after heart transplantation has been elucidated. Whereas recipients with less than a moderate degree of TR usually have a benign course, a considerable degree of TR may cause intractable right heart failure, which itself may contribute to early and late morbidity and mortality after heart transplantation [1, 29]. It is also natural that graft dysfunction due to rejection episodes possibly affects the occurrence and deterioration of TR during the follow-up period. Moreover, endomyocardial biopsies have been associated with the development of TR, presumably due to injury to the tricuspid valve cords [23, 30]. In the present study, both prevalence and severity of TR diminished 1 year after transplantation. It is also confirmed that early TR was not a risk factor for graft survival. Indeed, several recipients showed the development of TR from grade 1 to grade 2 during the total follow-up period. Although we could not find a significant correlation between those recipients and their rejection episodes or the number of endomyocardial biopsies, there might be some influences of those events on the development of posttransplant TR in the long term. Hence, additional follow-up should be continued to document the etiology of the development of later TR and long-term outcome.
In conclusion, TR observed early after neonatal heart transplantation occurs frequently. It is seldom of clinical significance and does not contribute to early or late graft loss. Oversized grafts resulting in atrial disproportion and prolonged ischemia were independent risk factors for TR. Although preoperative pulmonary hypertension was not a risk factor, transient right ventricular remodeling may occur to cope with intermittent early increases in afterload. Immediate posttransplant TR resolves in frequency and intensity over time. Recipient growth and convalescence from the perioperative ischemic effect were primary determinants of the resolution of TR.
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Acknowledgments
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We thank James Fitts and Joyce Johnston for gathering the data for this analysis, and we thank all members of the cardiac echocardiographic laboratory in Loma Linda University Children’s Hospital.
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References
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Abstract
Introduction
