行政院國家科學委員會專題研究計畫 成果報告
心臟移植後冠狀動脈疾病之疾病標的因子研究
計畫類別: 個別型計畫 計畫編號: NSC93-2314-B-002-268- 執行期間: 93 年 08 月 01 日至 94 年 07 月 31 日 執行單位: 國立臺灣大學醫學院外科 計畫主持人: 許榮彬 共同主持人: 蔡有光 報告類型: 精簡報告 處理方式: 本計畫可公開查詢中 華 民 國 94 年 10 月 30 日
Heart Transplantation in Patients with End-Stage Heart failure and Cardiac Ascites
Ron-Bin Hsu, MD
Department of Surgery, National Taiwan University Hospital, National Taiwan University
College of Medicine, Taipei, Taiwan, ROC
Short title: HTX and ascites
Category: original article
Word count:
Key words: heart transplantation, ascites
Address for reprints:: Dr. Ron-Bin Hsu, National Taiwan University Hospital, No.7,
Chung-Shan S. Rd. Taipei, Taiwan 100, R.O.C. Tel: 886-2-2312-3456 ext 5580.Fax:
ABSTRACT
Objective: Donor shortage and improved medical treatment of heart failure increase the
prevalence of patients with end-stage heart failure and cardiac ascites to heart transplantation.
The clinical outcome of heart transplantation in these patients has not been reported. Here, we
sought to evaluate the clinical outcome of heart transplantation in patients with end-stage
heart failure and ascites.
Methods: Data were collected by retrospective chart review.
Results: Between 1989 and 2005, 45 patients with end-stage heart failure and moderate to
severe ascites underwent orthotopic heart transplantation. There were 33 men and 12 women
with median age of 44 years (range 10-63 years). The causes of heart failure were congenital
heart disease in 4 patients (9%), dilated cardiomyopathy in 21 patients (47%), rheumatic
heart disease in 7 patients (16%), coronary artery disease in 10 patients (22%), and restrictive
cardiomyopathy and transplant coronary artery disease each in 1 patient. Twenty of 45
patients (44%) had previous cardiac operation. There were 10 in-hospital deaths (22%):
bleeding in 4 patients, sepsis with multiple organ failure in 5 patients and non-diagnostic
graft failure in 1 patient. Profuse postoperative bleeding requiring reoperation occurred in 14
patients (31%). The independent risk factors for hospital death were low serum albumin
(odds ratio, 0.05; 95% confidence interval, 0.003-0.591; p=0.018) and reoperation for
Conclusions: Heart transplantation in patients with end-stage heart failure and ascites was
associated with high hospital mortality and morbidity. The co-existence of cardiac ascites and
hypoalbuminemia implied poor prognosis.
Ultramini-abstract
Between 1989 and 2005, 45 patients with end-stage heart failure and ascites underwent
orthotopic heart transplantation. Heart transplantation in patients with end-stage heart failure
and ascites was associated with high hospital mortality and morbidity. The co-existence of
Introduction
The continuous improvement in clinical outcome after heart transplantation has established
heart transplantation as a standard and efficient therapy for end-stage heart failure [1].
Long-term survival is limited by transplant coronary artery disease and the complications
produced by the toxicities of maintenance immunosuppression [1-3]. In recent decades,
survival after heart transplantation is gradually improving, and there is increasing patient risk
profiles before transplantation [4]. The increasing patient risk profiles include previous
cardiac operations, use of mechanical assist devices, diabetes mellitus, critically ill recipients,
high pulmonary vascular resistance, prior sensitization, long allograft ischemic time, and use
of nonstandard or marginal donors [4]. Both donor shortage and improved medical treatment
of end-stage heart failure will increase the prevalence of patients with severe or late-stage
heart failure to heart transplantation. Right ventricular failure and cardiac ascites occur as late
complications of end-stage heart failure, and its development usually reduces patient survival
[5-7]. Cardiac ascites and cirrhosis might develop in patients with a long history of
congestive heart failure and systemic venous hypertension [8,9]. The clinical outcome of
heart transplantation in these patients has not been reported in series [10]. Here, we sought to
evaluate the clinical outcome of heart transplantation in patients with end-stage heart failure
and cardiac ascites.
Patients. A total of 241 consecutive patients underwent heart transplantation from June 1989
through July 2005 at National Taiwan University Hospital. Patients with moderate to massive
ascites before transplantation were included in this study.
Definitions. The diagnosis of cardiac ascites was based on clinical history, physical
examination and findings of abdominal sonography. Patients with liver cirrhosis secondary to
hepatitis virus infection or alcoholism were excluded from transplant candidates. The
diagnosis of liver cirrhosis was based on ultrasonic findings [11-13]. The cause of ascites was
considered as cardiac if patients had severe congestive heart failure and no evidence of
alcoholic or post-hepatitis liver cirrhosis. None of our patients received liver biopsy to
confirm the diagnosis of liver cirrhosis.
Data on age, sex, diagnosis of heart disease, renal and liver function tests, hemodynamics,
allograft ischemic time, and clinical outcome were recorded. Data of right atrial pressure,
transpulmonary gradient and pulmonary vascular resistance were derived from cardiac
catheterization. The severity of liver function impairment was graded according to the
Child-Pugh score [14].
Heart transplantation. All of the procedures of heart transplantation were performed
through a median sternotomy. The techniques of cardiopulmonary bypass were described
previously [15]. The operative techniques of heart transplantation in patients with prior
procedure. In patients with previous cardiac operation, we spent a liberal time for tissue
dissection and relief of dense adhesion. Preliminary exposure of femoral vessels was
performed in cases with a high risk of severe hemodynamic compromise during
re-sternotomy. Femorofemoral cardiopulmonary bypass can be instituted very rapidly if
needed.
Immunosuppression
All patients received triple-drug immunosuppressive therapy according to our heart
transplantation protocol previously described [16,17]. Since 1995, we started to use rabbit
antithymocyte globulins for induction therapy. Azathioprine (4mg/kg) was given one hour
before the operation. Solumedrol (1000mg) was infused while release of the aortic
cross-clamp. Rabbit antithymocyte globulin (1.5-2.5 mg/kg/day) was given after
transplantation for five days. Cyclosporine was started orally within five days after
transplantation or after the recovery of renal function. Cyclosporine dose was adjusted
according to renal function and serum cyclosporine level, which was maintained at the trough
level of 300-500 ng/ml during the first three months after transplantation and 200-300ng/ml
one year after transplantation. Azathioprine was given at 1-2 mg/kg/day after transplantation,
with the dose adjusted to maintain a white blood cell count 4000-6000/mm3. Prednisone
(0.5mg/kg/day) was started on the second postoperative day and tapered to 0.2 mg/kg/day by
(Cellcept) were used for recurrent rejection or severe adverse reactions to cyclosporine and
azathioprine. Since 2004, we started to use mycophenolate mofetil for primary
immunosuppression instead of azathioprine. To prevent nephrotoxicity, cyclosporine dose
was decreased to maintain serum trough level of 250-350 ng/ml during the first three months
after transplantation and 150-250 ng/ml one year after transplantation.
All patients were followed monthly at special cardiac transplantation clinic. Standard chest
roentgenogram, blood tests, electrocardiogram and physical examinations were routinely
performed at regular intervals.
Statistical analysis. The results are expressed as median with a range or as frequencies for
the categorical variables. Data analysis was performed using the Chi-squaretest,Fisher’s
exact test and Mann-Whitney test. Univariate and multivariate stepwise logistic regression
was used to identify independent risk factors for hospital death. The patient and graft survival
curve was plotted by the Kaplan-Meier method. Survival was compared by log-rank test
between patients with and without ascites. P ≤ 0.05 wasconsidered statistically significant.
Results
Patient characteristics. From 1989 through 2005, 241 patients with end-stage heart failure
underwent heart transplantation. There were 198 men and 43 women, and the median age was
49 years (range 0-71 years). The causes of heart failure were congenital heart disease in 8
patients (29%), and others. Eight patients received a re-transplantation and 4 patients received
combined heart-kidney transplantation. None of the patients had signs of chronic hepatitis
virus B or C infection. Chronic alcohol abuse was denied by all patients.
Forty-five patients with end-stage heart failure had moderate to massive ascites before
transplantation. The rate of transplant patients with ascites increased slightly from 14%
(14/102) during the 1989 to 1998 to 22% (31/139) during the 1999 to 2005. There were 33
men and 12 women, and the median age was 44 years (range 10-63 years). The causes of
heart failure were congenital heart disease in 4 patients (9%), dilated cardiomyopathy in 21
patients (47%), rheumatic heart disease in 7 patients (16%), coronary artery disease in 10
patients (22%), and restrictive cardiomyopathy and transplant coronary artery disease each in
1 patient. Patient demographics and laboratory data before transplantation were listed in
Table 1. Twenty of 45 patients (44%) had previous cardiac operation including 2 multiple
valve replacements, 1 coronary artery bypass surgery, 1 total cavopulmonary connection, 1
Fontan operation, 1 Rastelli operation, 1 heart transplantation, and 1 Senning operation. The
median level of serum total bilirubin was 1.9 mg/dl (range, 0.5 to 9.6); serum albumin, 3.4
g/dl (range, 1.4 to 4.8); serum blood urea nitrogen, 26 mg/dl (range, 9.6 to 109); serum
creatinine, 1.3 mg/dl (range, 0.49 to 11); serum asparate aminotransferase, 34 U/L (range, 12
to 223), and serum alanine aminotransferase, 21 U/L (range, 7 to 196). Twenty patients (44%)
abdominal sonography were moderate ascites in 23 patients and massive ascites in 22 patients.
Two patients had cardiac cirrhosis before transplantation. The median level of Child score
was 9 (range, 6 to 12).
Before transplantation, 13 patients were in UNOS status IA, 14 patient in UNOS status IB,
and 18 patients in UNOS status II. Before transplantation, 9 patients had endotracheal
intubation and mechanical ventilation, 4 patients had intra-aortic balloon pump, 5 patients
had mechanical support with extracorporeal membrane oxygenation, 1 patient had ventricular
assist device, and 4 patients required dialysis treatment because of anuria.
Among donors, there were 33 men and 12 women, and the median age was 27 years (range, 7
to 66). ABO blood types between donors and recipients were identical in 35 cases and
compatible in 10 cases. The body weight ratio between donors and recipients ranged from
0.72 to 1.74. The median duration of allograft ischemic time was 160 minutes (range, 40 to
320). All patients underwent orthotopic heart transplantation. One patient who had transplant
coronary artery disease and severe renal impairment underwent combined heart and kidney
transplantations.
Clinical outcomes. For all patients, there were 30 hospital deaths (12%). For 45 transplant
patients with cardiac ascites, there were 10 hospital deaths (22%) occurring between 1 and
152 days after transplantation (Table 1). Patients with cardiac ascites had a higher hospital
causes of hospital death in patients with cardiac ascites were bleeding in 4 patients, sepsis
with multiple organ failure in 5 patients and non-diagnostic graft failure in 1 patient. Profuse
postoperative bleeding requiring reoperation occurred in 14 (31%) of 45 patients with cardiac
ascites. Autopsy was performed in 4 of 10 patients with hospital death. Pathological
examination of the livers in these patients showed pictures of cardiac cirrhosis with
centrilobular necrosis and varying degree of fibrosis.
Follow-up was complete in all patients. The mean duration of follow-up was 50.6 ± 43.8
months. For all patients, the 6-month, 1-year, 3-year, 5-year, and 10-year patient and graft
survival rates were 86.2 ± 2.2%, 81.8 ± 2.5%, 71.0 ± 3.1%, 62.8 ± 3.5%, and 44.1 ± 5.3%.
For 45 patients with cardiac ascites, the 6-month, 1-year, 3-year, 5-year, and 10-year patient
and graft survival rates were 75.4 ± 6.4%, 70.1 ± 7.0%, 70.1 ± 7.0%, 61.6 ± 8.4%, and 51.2 ±
9.7% (Figure 1). For 196 patients without ascites, the 6-month, 1-year, 3-year, 5-year, and
10-year patient and graft survival rates were 88.7 ± 2.3%, 84.4 ± 2.6%, 71.4 ± 3.5%, 63.2 ±
3.9%, and 42.7 ± 6.1% (Figure 1). As shown in Figure 1, patients with cardiac ascites had
lower 6-month and 1-year patient and graft survival rates than patients without ascites. The
survival curves showed no difference since 3 years after transplantation.
Among patients with cardiac ascites, there were 7 late deaths. The causes of late death were
sudden death in 3 patients, sepsis with multiple organ failure in 2 patients, non-diagnostic
Risks of hospital death. As shown in Table 1, patients with hospital death had more
congenital heart disease, low recipient and donor body weight, low serum albumin, massive
ascites, low Child score, and high incidence of postoperative reoperation for bleeding. In
multivariate logistic regression analysis, the independent risk factors for hospital death were
low serum albumin (odds ratio, 0.05; 95% confidence interval, 0.003-0.591; p=0.018) and
reoperation for bleeding (odds ratio, 30.11; 95% confidence interval, 2.38-380.26; p=0.009).
Discussion
Heart transplantation. The clinical outcome of heart transplantation is improving. The
30-day survival rate improved from 84% during the early 1980 to 91% during the late 1990
[1]. The overall 1-year, 5-year and 10-year survival rates for heart transplantation were 80%,
70% and 50% [1]. However, the long-term survival remains unchanged in spite of the
ongoing stepwise improvement in early transplant survival. The survival rate for the entire
patient cohort of the worldwide registry showed that, after the steep fall in survival during the
first 6 months, the survival decreases at a linear rate of 3.4% per year [18]. We had a similar
result with the hospital survival rate of 88% and the 1-year patient and graft survival rate of
81.8%.
In view of increasing donor shortage, it is imperative to allocate organs to patients with the
greatest need and the greatest chance to derive the maximum benefit [19]. But, the quest for
over-selective in transplant candidates [20]. The risk factors for early mortality included old
donor age, old recipient age, having congenital heart disease or coronary artery disease as the
indication for heart transplantation, requiring mechanical circulatory support (temporary or
pulsatile ventricular assist device), mechanical ventilation, or dialysis at the time of transplant,
hospitalized at transplant, prolonged allograft ischemic time, and renal or hepatic dysfunction
at the time of transplant [18]. However, the impact of cardiac ascites on the survival of heart
transplantation has not been evaluated. In this study, we first demonstrated that the presence
of moderate to massive cardiac ascites at the time of transplant was a significant risk factor
for hospital death and early mortality after heart transplantation. The significant reduction of
patient and graft survival was sustained till 3 years after transplantation.
Ascites. Cardiac ascites and cirrhosis usually develop in patients with a long history of
congestive heart failure [5-9]. The occurrence of signs and symptoms of right ventricular
failure with ascites and high right atrial pressure is a well-known poor prognostic sign in
patients with end-stage heart failure. In a previous study, patients with a right atrial pressure
> 12 mmHg had a 47% 1-year survival rate as compared with the 68% survival rate for those
with a right atrial pressure < 12 mmHg [21]. Elevated right atrial pressure resulting from
right ventricular failure was also associated with a significantly increased risk of early death
after heart transplantation [22]. In addition, liver insufficiency with prolonged prothrombin
predictor of early death after heart transplantation [23]. Prolonged right ventricular failure
and systemic venous hypertension will lead to cardiac cirrhosis. Severe bleeding and
infection were usually the terminal events. Cardiac cirrhosis was found at autopsy in 75% of
the early deaths of heart-lung transplant recipients with right ventricular failure and
hyperbilirubinemia [24]. In our study, 31% of patients with cardiac ascites required
reoperation for profuse postoperative bleeding. Bleeding and sepsis accounted for 9 of 10
hospital death in patients with cardiac ascites. Although preoperative abdominal sonography
in 43 of 45 patients with cardiac ascites showed no liver cirrhosis, congestive liver fibrosis
(cardiac cirrhosis) was confirmed in 4 patients on postmortem pathological examination.
Cardiac cirrhosis is a clinically silent disorder characterized by a spectrum of morphologic
alterations in the liver ranging from mild deposition of sinusoidal collagen to emergence of
broad fibrous septa [25,26]. Occurrence of cardiac ascites is the hallmark of cardiac cirrhosis
[9]. Laboratory tests have a little role in the diagnosis of cardiac cirrhosis. In the majority of
patients with cardiac cirrhosis, serum levels of liver enzymes, bilirubin, and albumin are
within the normal range [9]. Ascites is also a manifestation of congestive heart failure and
reflects longstanding systemic venous hypertension. The clinical pictures of cardiac cirrhosis
usually are masked by symptoms and signs of right ventricular failure. A liver needle biopsy
may be required to evaluate the presence and severity of cardiac cirrhosis in patients with
Hypoalbuminemia. Child-Pugh score is significantly associated with hepatic
decompensation and mortality after cardiac surgery in patients with cirrhosis. Patients with a
Child-Pugh score ≧ 8 have a high mortality rate of 67% [27]. In this study, Child-Pugh
score was associated with a high hospital mortality rate (Figure 1).
Preoperative serum albumin was used to quantify nutritional status and underlying disease.
An albumin level of less than 2.5 g/dL was independently associated with increased risk of
reoperation for bleeding, postoperative renal failure, and prolonged ventilatory support,
intensive care unit stay, and total length of stay after cardiac surgery [28]. Hypoalbuminemia
was a powerful risk factor for perioperative complications in elderly patients and children
undergoing cardiac surgery [29,30]. Dichtl et al [31] reported no perioperative mortality after
heart transplantation in patients with cardiac hepatopathy and normal plasma protein levels.
In our study, hypoalbuminemia was the most powerful risk factor for hospital death after
heart transplantation. Nine of 25 patients (36%) with cardiac ascites and serum albumin < 3.5
g/dl had hospital death, and only 1 of 20 patients (5%) with ascites and serum albumin > 3.5
g/dl had hospital death. The co-existence of cardiac ascites and hypoalbuminemia was
associated with poor hospital outcome.
Study limitation. This study was limited by small case number and retrospective study. In
addition, the duration of right ventricular failure was unknown and the diagnosis of cardiac
complications in patients with advanced liver dysfunction [32]. Although our results were
preliminary, this was the first study of heart transplantation in patients with end-stage heart
failure and cardiac ascites. Patients should be carefully selected for heart transplantation,
especially in patients with cardiac ascites and serum albumin < 3.5 g/dl. Because the hospital
mortality rate was not low in patients with cardiac ascites and normal serum albumin, we
recommended that an invasive liver biopsy may be indicated only in patients with cardiac
ascites and hypoalbuminemia before transplantation.
Conclusions. Heart transplantation in patients with end-stage heart failure and ascites was
associated with high hospital mortality and morbidity. The co-existence of cardiac ascites and
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Table 1. Patient characteristics in 45 patients with cardiac ascites: comparison between patients with and without hospital death by Fisher exact test and Mann-Whitney U test.
Variables Died (n=10) Alive (n=35) P-value
Male 5 (50%) 28 (80%) 0.101
Median age in years (range) 40 (17-60) 45 (10-63) 0.4443
Diagnosis of heart disease
Dilated cardiomyopathy 2 (20%) 19 (54%) 0.078
Coronary artery disease 2 (20%) 8 (23%) 0.999
Rheumatic heart disease 3 (30%) 4 (11%) 0.172
Congenital heart disease 3 (30%) 1 (3%) 0.03
Others 0 3
Body weight in kilograms 48.95 (32-65) 59.8 (23-100) 0.026
Blood type-identical 8 (80%) 27 (77%) 0.999
Previous cardiac operation 7 (70%) 13 (37%) 0.083
Diabetes mellitus 3 (30%) 6 (17%) 0.393
Donor-age in years 25.5 (12-66) 27 (7-58) 0.6324
Donor-male 7 (70%) 26 (74%) 0.999
Donor-body weight in kilograms 55 (45-70) 65 (20-85) 0.0105 Recipient/donor body weight ratio 1.1 (0.78-1.5) 1.08 (0.72-1.74) 0.5755
Serum albumin (g/dl) 2.8 (1.4-3.73) 3.7 (2.2-4.8) 0.0005
Serum total bilirubin (mg/dl) 1.1 (0.5-6.27) 2.1 (0.5-9.6) 0.6522 Serum asparate aminotransferase (U/L) 37.5 (16-96) 34 (12-223) 0.7431 Serum alanine aminotransferase (U/L) 21.5 (9-72) 21 (7-196) 0.6036 Serum blood urea nitrogen (mg/dl) 29 (13.7-85) 24.3 (9.6-109) 0.6039 Serum creatinine (mg/dl) 1.25 (0.6-3.19) 1.3 (0.49-11) 0.8695 Prothrombin time prolongation > 4 seconds 3 (30%) 17 (49%) 0.473
Ascites-massive 8 (80%) 14 (40%) 0.035
Child-Pugh score 9.5 (7-12) 8 (6-12) 0.0286
UNOS status IA or IB 7 (70%) 20 (57%) 0.606
Right atrial pressure 19 (8-26) 20 (6-36) 0.902
Transpulmonary gradient 9 (4-20) 8 (0-28) 0.6614
Figure legends
Figure 1. Patient and graft survival curves plotted by Kaplan-Meier method in patients with