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Ann Thorac Surg 1995;59:1134-1140
© 1995 The Society of Thoracic Surgeons

Tricuspid Valve Regurgitation Attributable to Endomyocardial Biopsies and Rejection in Heart Transplantation

Divisions of Thoracic and Cardiovascular Surgery and Cardiology Surgical Center, Hannover Medical School, Hannover, Germany

Accepted for publication January 20, 1995.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
In the present report the prevalence, severity, and risk factors of tricuspid valve regurgitation (TR) in 251 heart transplant recipients have been analyzed retrospectively. Tricuspid valve function was studied by color-flow Doppler echocardiogram and annual heart catheterization. The presence or severity of TR was graded on a scale from 0 (no TR) to 4 (severe). Additional postoperative data included rate of rejection, number of endomyocardial biopsies, incidence of transplant vasculopathy, and preoperative and postoperative hemodynamics. The incidence of grade 3 TR increases from 5% at 1 year to 50% at 4 years after transplantation. Multivariate analysis showed rate of rejection and donor heart weight to be significant risk factors. The ischemic intervals as well as the preoperative and postoperative pulmonary hemodynamics did not affect the severity or prevalence of TR. These results indicate that various factors appear to have an impact on the development of TR and that the prevalence might be lowered by a reduction of the number of biopsies performed and when possible, oversizing of donor hearts.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Tricuspid valve regurgitation (TR) has been recognized as a frequent postoperative sequela in orthotopic cardiac transplantation. The prevalence of TR in a number of studies varies from 40% to 85% [1] and both prevalence and severity increase with the length of the postoperative course [2]. Some of these patients with symptoms of systemic venous congestion require intensive medical treatment and ultimately, operation [3, 4].

Uncertainty exists as to the actual cause of TR. Various factors are discussed, such as the type of surgical anastomosis of the right atrium [5], number and severity of rejection episodes, chordal damage [6, 7] and rupture caused by endomyocardial biopsies [7], degree of preoperative or postoperative pulmonary vascular resistance, and pulmonary artery pressure [8]. In addition distortion of the cardiac geometry of donor hearts in enlarged pericardial cavities may perpetuate the development of TR [9].

The purpose of this retrospective study is to determine the prevalence and severity of TR as well as the significance of different risk factors in the development of TR based on a study population of patients who received transplants at the Hannover Medical School.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Between April 1986 and October 1993, 425 patients received a heart transplant at the Hannover Medical School. To evaluate the long-term significance of TR a minimum postoperative follow-up of 1 year was required for enrollment in this study. After 174 patients had been excluded either because of early postoperative death (n = 65), a follow-up of less than 1 year (n = 45), or the patient transferring to a different medical center for clinical follow-up (n = 64), the remaining 251 patients (33 women; 218 men) with a average follow-up of 1,399 ± 703 days (range, 375 to 4,663 days) were analyzed with respect to presence and severity of TR.

Evaluation of Tricuspid Valve Regurgitation
The standard annual invasive cardiologic examination consisted of routine right and left heart biplane angiography and coronary angiography, right and left ventricular pressure tracings, and the thermodilution technique for cardiac output determination. In addition, two-dimensional and Doppler echocardiographic studies were performed using standard techniques (Hewlett Packard Echocardiography; 3.5 MHz phased-array transducer) [10]. The regurgitant jet was visualized by color Doppler echocardiography in systole during inspiratory hold. The ratio of maximal length and maximal area of the tricuspid regurgitant signal in relation to the right atrial area was then calculated. The echocardiographic evaluation also included a two-dimensional assessment of the tricuspid valve structure. The echocardiographic results were compared with atrial and ventricular pressure curves obtained during heart catheterization.

The semiquantitative grading of TR was based on the results of all above diagnostic studies: grade 0 = no TR; grade 1 = mild TR; systolic jet just detectable, ratio 0 to 0.2; grade 2 = moderate TR; systolic jet less than mid right atrial area, ratio 0.3 to 0.5; grade 3 = moderate to severe TR; systolic jet more than mid right atrial area, ratio 0.6 to 0.8; and grade 4 = severe TR; jet filling right atrium completely; retrograde flow in hepatic veins, ratio more than 0.8, severe symptoms of systemic venous congestion (ratio is calculated as the maximal regurgitant jet area to the right atrial area by echocardiography).

Grading of TR was performed at least once a year during the annual catheterization and the patients were classified according to the degree of TR based on the worst grading during the postoperative course. As the number of patients with grade 4 TR was very small (n = 6) the data of these patients were summarized in the results of grade 3 TR patients.

Immunosuppression Protocol
Standard perioperative immunosuppression consisted of methylprednisolone and prophylactic T-cell antibodies (RATG, OKT3). Maintenance immunosuppression consisted of oral triple drug immunosuppression with prednisolone, azathioprine, and cyclosporine. Target-specific cyclosporine trough levels for the first postoperative year were 250 to 300 ng/mL. Allograft rejections were treated with pulse steroid boluses (methylprednisolone, 500 mg/day for 3 days), or in patients with recurrent rejection with polyclonal or monoclonal antibodies (RATG, OKT3) and subsequent steroid taper from 60 to 10 mg/day over 60 days.

Other Prophylactic Measures
To prevent right ventricular distention or right ventricular failure during the immediate postoperative period all patients received intravenous inotropic support (dopamine, adrenaline) and as necessary, intravenous nitrates (glyceroltrinitrate), prostaglandins (prostacycline), or phosphodiesterase inhibitors (enoximone). In addition patients with a temporary loss of sinus node function or an atrioventricular conduction disturbance were temporarily paced with atrial or ventricular wires, or both, placed during the operation at a minimum rate of 80 to 100 beats/min for the first 7 postoperative days to minimize diastolic right ventricular distention. Continuous sinus node or atrioventricular nodal dysfunction resulted in the implantation of a permanently placed ventricular pacemaker.

Since 1988 a reduction of the pericardial cavity was performed in those patients with enlarged pericardial sacs in relation to the size of the implanted donor heart. Tight pericardial closure was only omitted if this procedure threatened to impair right ventricular function in patients with initial right ventricular dysfunction. Reduction of the pericardial cavity was performed in 71 (28%) of the 252 patients analyzed in this study.

Detection and Grading of Acute Rejection
Detection and monitoring of acute rejection was accomplished by transvenous endomyocardial biopsies graded according to the Hannover classification [11]. During each biopsy procedure five to seven endomyocardial specimens were retrieved using the standard bioptom under fluoroscopic vision. The biopsy specimens were obtained from the interventricular septum near the apex. Scar tissue formation sometimes required biopsy specimens to be taken from the interventricular septum closer to the pulmonary outflow tract. During the first months after transplantation the minimal interval between positive biopsies after a rejection was 1 week and this interval was lengthened with increasing duration of the postoperative course according to standard biopsy scheme [12]. By the end of the first year the average interval between biopsies was 4 weeks and every 3 months until postoperative year 4. Treatment was instituted in patients with moderate or severe rejection (grade 3b, grade 4, Hannover classification). After 3 years biopsies were replaced by echocardiographic evaluation and nuclear imaging in selected patients with a rejection-free interval of more than 360 days.

Evaluation of Transplant Vasculopathy
The incidence of transplant vasculopathy was evaluated by annual coronary arteriograms. A histiopathologic examination was done on deceased patients. Standard projections were noted and replicated on subsequent arteriography. Vasodilatation was standardized by administration of nitroglycerine into the coronaries during the procedure. The angiograms were analyzed visually and were compared side-by-side (consensus of two observers) with special attention to the presence of minimal coronary vascular changes in all branches of the vascular tree. Coronary artery disease was defined as any narrowing of the coronary vessels. Stenosis were fully categorized according to the description of Gao and associates [13] as focal, diffuse concentric narrowing, or abrupt ending of the terminal branches.

Statistical Analysis
Patient data were analyzed with the Statistical Program of Social Sciences (SPSS for Windows, version 6.0; Birmingham, AL). Continuous data were expressed as mean ± standard deviation and the individual grades of TR were compared to each other by analysis of variance using the Scheffé method. The correlation of the different grades of TR to the measured parameters was performed using the Kendall correlation analysis. For a qualitative multivariate covariance analysis a discriminant function analysis according to the Wilk's lambda method was used. Mortality was analyzed as actuarial data according to the method developed by Kaplan-Meier.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
The general group characteristics in terms of follow-up, sex, and age are depicted in Table 1. One year after heart transplantation TR grade 3 was recognized in 6% of the patients, a year later in 16%, and after 4 years in 50% of the patients. At 4 years after transplantation less than 4% of the patients were free of TR (Fig 1).

View larger version (53K): [in this window] [in a new window]   Fig 1. . Distribution of various grades of tricuspid valve regurgitation (TR) over a 6-year posttransplantation period. A significant increase in prevalence of grade 3 TR.

View larger version (24K): [in this window] [in a new window]   Fig 2. . Mean pulmonary arterial pressure (MPAP) and cardiac index (CI) at the time when the worst grade of tricuspid valve regurgitation (TR) experienced by each patient was first registered. The difference in CI between patients with grade 0 and grade 3 TR is significant by ANOVA and correlation analysis.

Our analyses of the preoperative recipient pulmonary vascular resistance index (PVRI) and systolic pulmonary pressure (SPAP) showed a similar PVRI and SPAP for all grades of TR (Fig 3). In our study population patients with a preoperative SPAP of more than 55 mm Hg had a similar prevalence of moderate to severe or severe TR as patients with an SPAP of less than 55 mm Hg (SPAP 55 mm Hg or less grade 3/4 TR, 33%; SPAP more than 55 mm Hg grade 3 TR, 25%; p = not significant [NS]). Patients without TR had a preoperative mean SPAP of 24 ± 6 mm Hg, whereas patients with grade 3/4 TR had a SPAP of 25 ± 7 mm Hg (p = NS).

View larger version (25K): [in this window] [in a new window]   Fig 3. . Influence of preoperative systolic pulmonary artery pressure (SPAP) and preoperative pulmonary vascular resistance index (PVRI) on the severity of tricuspid valve regurgitation (TR).

A detailed analysis of the recipient weight at the time of transplantation in relation to the donor weight revealed that recipients with hearts from donors weighing more than the recipient were less likely to develop TR than vice versa. Figure 4 correlates the weight difference between recipient and donor to the presence and severity of TR. In patients without TR (grade 0) the average donor was 3.3 ± 10 kg heavier than the recipient, whereas patients with TR grade 3 were an average of 6.7 ± 12 kg heavier than the donor (p < 0.05). The Kendall correlation coefficient was 0.245 (p < 0.01). Figure 4 also shows the influence of donor age on the development of TR. The average donor age in patients without TR was 23.3 ± 8.1 years and 26.2 ± 6.9 years in patients with grade 3 or 4 TR (p = NS).

View larger version (16K): [in this window] [in a new window]   Fig 4. . Calculation of recipient minus donor body weight as well average donor age in respect to grade of tricuspid valve regurgitation (TR). The prevalence of grade 3 TR is far less in patients having received a heart from a donor heavier than the recipient.

There is a significant correlation between the number of biopsies taken during the first postoperative year and the development of TR as outlined in Figure 5. Patients with TR grade 3 had an average of 29 ± 9 biopsies taken compared with an average of 21 ± 8 biopsies in patients without TR (p < 0.05). After the third postoperative year 39% of the patients with more than 30 endomyocardial biopsies performed during the first postoperative year experienced grade 3 TR, opposed to 14.5% with less than 30 endomyocardial biopsies (p < 0.05). In 8 patients with mild TR an increase in the severity of TR to grade 2 or grade 3 was recognized immediately after an endomyocardial biopsy. In all of these patients the biopsies were negative for rejection. Echocardiographic evaluation showed structural changes in the chordal apparatus of the tricuspid valve. The number of biopsies performed correlates with the degree of TR present (r = 0.34; p < 0.01).

View larger version (28K): [in this window] [in a new window]   Fig 5. . Frequency of rejection episodes and number of biopsies by the end of the first postoperative year and their influence on the prevalence and severity of tricuspid valve regurgitation (TR). Patients with frequent rejection and large number of endomyocardial biopsies performed have a significantly higher prevalence of moderate to severe TR.

Table 4 shows the impact of pericardial reduction plasty on the relative incidence of TR at the time when the worst grade of TR experienced by each patient was first registeredtab 4. The long-term analyses showed that the pericardial reduction plasty did not significantly affect the severity or prevalence of tricuspid incompetence (Kendall correlation coefficient = 0.08; p = NS).

The 6 patients with grade 4 TR summarized in the analysis with grade 3 TR patients showed typical symptoms of systemic venous congestion such as the development of ascites, pleural effusions, and peripheral edema. So far all of these patients have received surgical treatment. The intraoperative findings revealed significantly torn or ruptured chordae and valvular structures in 3 of the 6 patients. Valve replacement was performed using a biologic prothesis in 2 patients. In the remaining 4 patients valve reconstruction was possible. At first, the functional results of the tricuspid valve reconstruction was fairly good with only minimal incompetence (grade 1 to 2); however, late follow-up (more than 12 months) revealed moderate to severe TR (grade 3 TR) in all patients after reconstruction. The postoperative course of patients undergoing valve reconstruction was often quite severe.

Mortality increases with severity of TR. Patients with grade 3 or 4 TR have a 15% actuarial mortality at 2 years compared to 6% actuarial mortality in patients without TR (p < 0.05).

The discriminant function test for a multivariate analysis of all independent parameters showed only the number of biopsies performed during the first postoperative year, the weight difference between recipient and donor and the cardiac index to be significant parameters for the prediction of TR.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Tricuspid valve regurgitation is a postoperative complication that affects more than 50% of the cardiac transplant population within the first year after transplantation (Fig 1). Fortunately in most patients only severe TR is associated with secondary cardiac insufficiency and associated symptoms such as peripheral edema or hepatic and renal functional impairment. The prevalence and severity of TR increases with time after transplantation (Fig 1). Five years after transplantation none of the patients in our study were free of TR, more than 80% with grade 2 or grade 3 TR. Unfortunately this underlines the long-term impact and seriousness of this postoperative complication.

Various individual factors have been made responsible for the presence of TR in heart transplant recipients. This includes distortion of the right atrial anatomy due to the type of conventional anastomosis, typically using a cuffed anastomosis of the donor and recipient atrium [14, 15]. In a report of two successful cases Sievers and colleagues [5] have not seen TR 2 weeks postoperatively using bicaval anastomosis of the right atrium. This type of alternative surgical procedure leaves the donor right atrium completely intact, thereby avoiding distortion of the natural geometry, a factor that could be responsible for later development of TR. Tricuspid regurgitation is very uncommon in heart-lung transplanted patients, a group in which the right atrial anastomosis is identical to heart transplant patients. This may indicate that the type of anastomosis may not be the primary determinant in the development of TR.

Reduction of the pericardial cavity to decrease the severity of TR in heart transplant recipients has proved beneficial in short-term follow-up as shown by Haverich and associates in 1991 [9]. In theory this procedure would prevent distortion of the donor heart in an enlarged pericardial sac [1], preserve the natural shape of the valve, and eventually result in improved atrioventricular valve competence. In contrast to the early report the present investigation demonstrates that the long-term results regarding the incidence of TR were not affected by this type of surgical intervention (Table 4). Again this is underlined by the fact that in patients after heart-lung transplant the pericardium is often left open or resected and nevertheless these patients very rarely suffer from any significant degree of TR.

According to Lewen and colleagues [8] patients with an elevated preoperative SPAP of more than 55 mm Hg are more likely to experience TR in the early postoperative period. In our study population there was no positive correlation to TR between the preoperative PVRI or the preoperative SPAP (Fig 3). The difference in results can be explained by a tendency in our group to supply recipients with significantly elevated preoperative pulmonary vascular resistance (PVR) with oversized donor hearts as well as a careful fluid balance and inotropic support with intravenous adrenaline for a minimum of 3 days postoperatively to prevent delayed onset of right heart failure. Lewen and associates [8] also found a higher incidence of TR in patients with a postoperative PVR in excess of 240 dynes • s • cm^-5. According to our data there was a constant, steady and significant rise of the PVRI parallel to the severity of TR and it remains unclear if this is simply the result of the TR and a drop in forward cardiac index or actually one of the possible causes of TR.

Postoperative cardiac function is related directly to the number and severity of allograft rejections [16]. A careful determination of the rate of rejection per postoperative day and the number of rejections during the first and crucial postoperative year clearly points out the significance of rejection for development and progression of TR. The average rate of rejection is more than doubled in patients with grade 3 TR in comparison to patients without TR (Fig 5). Allograft rejection, especially during the initial postoperative period can severely affect myocardial function with dilatation, myocardial stiffness, dyskinesia, and paradoxic septal motion [17, 18], all of which adversely affect valvular function [19]. These changes can be permanent [20] and therefore, valvular dysfunction may not improve with time. We have seen grade 3 TR in a number of patients with severe postoperative right heart failure or therapy-resistant rejection as early as 2 months after transplantation.

Patients with a high rate of rejection episodes are also subjected to a high frequency of endomyocardial biopsies. This invasive procedure may cause damage of the valve leaflets, chordal structures, and papillary muscles. Echocardiographic evaluation showed an incidence of chordal or leaflet damage in 18% of the patients with grade 3 or 4 TR. In our series, patients with grade 3 TR had an average of 29 ± 9 biopsies during the first postoperative year compared to 21 ± 8 biopsies in patients without TR (p < 0.05 ; Fig 5). Of 6 patients that have undergone tricuspid replacement or reconstruction, the chordal apparatus of the tricuspid valve was severely damaged in 3. In 8 patients an increase in the severity of TR was recognized immediately after an endomyocardial biopsy procedure, thus underlining the significant impact of this invasive procedure for the development of TR. These results are in accordance with previously published data [7, 21] and undoubtedly warrant a more careful indication for and performance of endomyocardial biopsies. The chance of structural damage increases significantly with the number of biopsies performed. Certainly the average number of such procedures performed in this study population could explain the high incidence of TR. Again these statistics are supported by data from heart-lung transplant patients, which infrequently show any degree of TR. These patients are very rarely exposed to endomyocardial biopsies and it is a general understanding that cardiac rejection in heart-lung transplantation is an uncommon finding [22].

In 1991 Costanzo Nordin and colleagues [23] published an article on the benefits and disadvantages of oversizing donor hearts. Their conclusion was that undersizing does not necessarily negatively affect patient outcome in respect to myocardial contractility and adaptation to increased preoperative PVR. Our analyses of the influence of recipient to donor weight on the incidence of TR showed a negative impact of undersizing donor hearts. Oversized donor hearts were significantly less likely to develop TR (Fig 4). Therefore, one may speculate that an oversized heart may be more likely to cope with a preoperatively elevated PVR, thus be less prone to failure, dilatation with subsequent development of TR.

In agreement with other investigators we have not found a correlation between the incidence of TR and the ischemic time of the transplanted organ [24]. Transplant vasculopathy was present in only 13% of the patients without TR, whereas 27% of the patients with grade 3 TR showed evidence of transplant vasculopathy. Most likely coronary vasculopathy may be more a result of the high incidence of rejection in the patients with grade 3 TR than the actual cause of valvular leakage, although this remains to be proved.

According to our data pacemaker implantation did not affect the prevalence of TR. In all grades of TR approximately 16% to 25% of the patients required implantation of a pacemaker of which less than 10% remained pacer dependent.

For this analysis TR was graded according to color Doppler echocardiography and right atrial and ventricular pressure measurements during heart catheterization in a semiquantitative fashion. In the literature there is still no agreement about the quantitative assessment of the severity of any valve regurgitation and there continues to be a concern about the capability of color Doppler to quantify the severity of tricuspid lesions. We are aware of these difficulties and, therefore, have attempted to control the Doppler analysis with hemodynamic measurements and two-dimensional echocardiographic assessment of valve structure. Still this may have resulted in a significant degree of misgrading, false negative or positive results, and overlooking of structural valve defects.

In conclusion, tricuspid valve incompetence is present in a significant number of patients after heart transplantation. The prevalence increases with duration after transplantation. Various factors may affect the prevalence and severity of TR. The development of TR increases with the rate of rejection, number of biopsies taken, and undersizing the donor heart. Attempts to avoid TR by pericardial reduction plasty have failed in long-term follow-up. The value of changing the operative technique of transplantation by using bicaval anastomosis is presently uncertain. At the moment aggressive rejection treatment and oversizing the donor heart seem to be useful in limiting the incidence and severity of TR. As structural defects can most certainly be attributed to endomyocardial biopsies, these procedures should be performed very carefully and as seldom as necessary.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Presented at the Twentieth Annual Scientific Meeting of the Society of Transplant Surgeons, Chicago, IL, May 18–20, 1994

Address reprint requests to Dr Hausen, Division of Thoracic and Cardiovascular Surgery, Hannover Medical School, Org.Nr. 6210, D-30623 Hannover, Germany.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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21. Reddy SC, Rath GA, Ziady GM, Matesic C, Kormos R. Tricuspid flail leaflets after orthotopic heart transplant: a new complication of endomyocardial biopsy. J Am Soc Echocardiogr 1993;6:223–6.[Medline]
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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hausen, B. Articles by Schäfers, H.-J. Search for Related Content PubMed PubMed Citation Articles by Hausen, B. Articles by Schäfers, H.-J.