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Ann Thorac Surg 2006;81:522-529
© 2006 The Society of Thoracic Surgeons
Cardiothoracic Centre, All India Institute of Medical Sciences, New Delhi, India
Accepted for publication August 15, 2005.
* Address correspondence to Dr Chowdhury, All India Institute of Medical Sciences, New Delhi 110029, India (Email: ujjwalchow{at}rediffmail.com).
| Abstract |
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METHODS: Three hundred ninety-five patients undergoing pericardiectomy for constrictive pericarditis between January 1985 and December 2004 were studied. Age was 10 months to 71 years (mean, 25.1 ± 13.4 years). Three hundred thirty-eight patients (85.6%) underwent total pericardiectomy (group I), and 57 patients (14.4%) underwent partial pericardiectomy (group II).
RESULTS: Operative and late mortality rates were 7.6% and 4.9%, respectively. Preoperative high right atrial pressure, hyperbilirubinemia, renal dysfunction, atrial fibrillation, pericardial calcification, thoracotomy approach, and partial pericardiectomy were significant risk factors for death. The risk of death was 4.5 times higher (95% confidence interval: 2.05 to 9.75) in patients undergoing partial pericardiectomy. At a mean follow-up of 17.9 ± 0.3 years (95% confidence interval: 17.3 to 18.6), actuarial survival was 83.8% ± 0.04% in group I and 73.9% ± 0.06% in group II (p = 0.004). At their last follow-up, 96.3% survivors of group I and 79.1% survivors of group II were in New York Heart Association class I/II (p < 0.001).
CONCLUSIONS: Total pericardiectomy is associated with lower perioperative and late mortality, and confers significant long-term advangage by providing superior hemodynamics that appear to be independent of the etiology of constrictive pericarditis.
| Introduction |
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This study aims to first, evaluate the results of total versus partial pericardiectomy clinically, echocardiographically and hemodynamically; second, determine the extent of resection that can be achieved with either thoracotomy or sternotomy approach; and third, determine the predictors of early and long-term survival after surgery for tuberculous and nontuberculous constrictive pericarditis.
| Patients and Methods |
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The surgical approach was based on surgeon preference and remained uniform throughout the study period. However, a left anterolateral thoracotomy was the preferred option in the setting of purulent pericarditis to avoid sternal infection. The median sternotomy approach was preferred in the following cases: (1) annular constrictive pericarditis, (2) calcific pericardial patch compressing the right atrium and right ventricular outflow tract, (3) extracardiac intrapericardial mass, (4) presence of a gradient between the superior and inferior venae cavae and right atrium 2 mm Hg or greater, (5) constriction after previous open heart surgery, and (6) recurrent constrictive pericarditis after partial pericardiectomy.
Patient Characteristics
Between January 1985 and December 2004 at our institution, 395 consecutive patients (276 males) underwent pericardiectomy for constrictive pericarditis (Fig 1). Their records were reviewed for demographic, operative, and perioperative features, follow-up echocardiographic, catheterization and clinical data (Tables 1, 2). Age ranged from 10 months to 71 years (mean, 25.1 ± 13.4 years; median, 24). Duration of symptoms ranged from 15 days to 6 years (mean, 20 ± 8.6 months). The majority were in New York Heart Association (NYHA) class III/IV (n = 389, 98.2%); 97.7% had distended jugular veins, 92.4% ascites, 87.3% hepatomegaly, 47.5% pleural effusion, and 27.6% pulsus paradoxus. Of 188 patients, 156 (82.9%) with pericardial effusion required tapping and steroid therapy. All patients with tuberculosis (n = 351) received multidrug therapy (isoniazid, rifampicin, ethambutol, and pyrazinamide) for an initial 3 months followed by triple-drug therapy for at least 9 months after operation. The interval between pericardial effusion and development of constriction ranged from 1 to 12 months (mean, 6.3 ± 3.6). Before the operation, all patients were on digitalis and diuretics. Twenty-one patients (5.3%) underwent emergency pericardiectomy through left thoracotomy. These patients had pyogenic or effusive-constrictive pericarditis not resolving with pericardiocentesis.
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Laboratory investigation showed elevated erythrocyte sedimentation rate (range, 40 to 80 mm at 1 hour) in 104 patients (26.3%), and renal dysfunction (creatinine > 2.0 mg/dL) in 42 patients (10.6%). Hypoalbuminemia was found in 140 patients (35.4%) and hyperbilirubinemia in 84 patients (21.2%). Chest roentgenogram revealed cardiomegaly (n = 134, 33.9%), pericardial calcification (n = 130, 32.9%), pleural effusion (n = 188, 47.5%), and pulmonary infiltrates (n = 132, 33.4%). The calcification was distributed on the anterior and inferior surfaces of the heart in 87 patients, on the posterior surface in 28, and in the atrioventricular groove in 15 patients. Electrocardiogram demonstrated low-voltage QRS complex (n = 100), flattening or T-wave inversion (n = 86), atrial fibrillation (n = 71), and premature ventricular contractions (n = 7).
Echocardiography revealed the following: pericardial thickening greater than 3 mm (n = 383), inferior venae cavae dilatation (n = 395), greater than 25% variation in mitral inflow velocity with respiration (n = 395), moderate mitral regurgitation (grade 2+, n = 124), moderate tricuspid regurgitation (grade 2+, n = 82), and extracardiac intrapericardial mass (n = 4).
Preoperative cardiac catheterization was performed in 353 patients (Table 2). The rest (n = 42) did not have catheterization because of their class IV symptoms with renal dysfunction. All demonstrated the findings considered diagnostic of constrictive pericarditis: an elevated right atrium pressure, usually with a M- or W-shaped contour; an abnormally high right ventricular end-diastolic pressure with a characteristic dip-plateau diastolic configuration; and a ratio of right ventricular end-diastolic to right ventricular systolic pressure of 0.30 or more.
Etiology
A specific etiologic factor was identified in 380 patients (96.2%). The etiology was considered tubercular if the histopathology of the excised pericardium showed granulomas, caseation, giant cells (n = 351, 88.9%), or if fluid and debris removed at surgery was positive for acid fast bacilli (n = 121). A history of pulmonary tuberculosis, lymph node tuberculosis, and skeletal tuberculosis was present in 188 (53.5%), 56 (15.9%), and 10 patients (2.8%), respectively.
The most common cause of purulent pericarditis (n = 25) was Staphylococcus aureus. Four patients (1%) presented with features of recurrent pericardial effusion and constriction due to malignancy. Histologically, they showed undifferentiated adenocarcinoma with lung (n = 2) and ovary (n = 2) as the primary site. Histologically, the idiopathic group (n = 15) showed dense fibrotic tissue with no evidence of tuberculosis. Constrictive pericarditis developed after mitral valve replacement in 7 patients, and after open mitral commissurotomy in 2 patients.
Definitions
Total pericardiectomy was defined as wide excision of the pericardium with the phrenic nerves defining the posterior extent, the great vessels including the intrapericardial portion of and superior vena cavaright atrium junction defining the superior extent, and the diaphragmatic surface, including the inferior vena cavaright atrium junction defining the inferior extent of the pericardial resection. Constricting layers of the epicardium were removed whenever possible. Any excision less than total was considered partial.
For uniformity with other studies constrictive pericarditis was considered to be hemodynamically significant when there were clinical features of constriction with supportive echocardiographic and hemodynamic criteria as outlined earlier. Perioperative mortality was defined as that occurring within 30 days after surgery. Cardiac-related death was defined as death due to cardiac causes, such as progressive congestive heart failure.
Surgical Technique
In 300 patients (75.9%), pericardiectomy was performed through a median sternotomy; and in 95 patients (24.1%), it was done through a left antrolateral thoracotomy. After median sternotomy, the pericardium was inspected and palpated to determine a relatively soft and uncalcified area. The thymus and pleural reflection was mobilized laterally to obtain a wide width of pericardium. An I-shaped incision was made over the pericardium. The thickened pericardium was incised using cautery until the parietal pericardium and underlying epicardial fat was located. This underlying fat often bulges through the incision. The incision was extended, and a cleavage plane between the thickened parietal and visceral pericardium was identified. This plane is typically avascular and superficial to the visceral pericardium. When calcified spicules or plaques penetrating the epicardium were present, we left behind islands of calcified pericardium. Circumferential patches of calcified pericardium were divided with rongeurs or a thick hemostat and was removed, avoiding injury to the phrenic nerves and the underlying vascular structures.
Attempts to decorticate the left side of the heart were made first. Pericardiectomy was performed between the phrenic nerves. The pericardium covering both ventricles, the great vessels, the venae cavae, and the right atrium was excised, avoiding injury to the phrenic nerve. Special precaution was taken to dissect and remove any constricted epicardial layers. The pericardium over the right atrium and venae cavae was resected last. Cardiopulmonary bypass was used in 7 cases, because of perforation of the inferior vena cavaright atrium junction (n = 4), pulmonary artery (n = 3), and massive bleeding.
Left anterolateral thoracotomy through the fifth intercostal space was performed in 95 patients. When chronic constrictive pericarditis was the indication for surgery (n = 57), the process of decortication was generally terminated on the left side as soon as the left atrioventricular groove was reached after mobilization and retraction of the left phrenic nerve. On the right side, the decortication was limited to the right atrioventricular groove. These patients (n = 57) underwent partial pericardiectomy according to the study criteria.
It was possible to achieve total pericardiectomy in all patients through sternotomy (n = 300) and a subset of patients through thoracotomy (pyogenic n = 25, 26.3%; effusive-constrictive n = 13, 13.6%).
Postoperative Assessment
Of 395 original patients, there were 30 perioperative (7.6%), and 18 late deaths (4.9%). Seven patients were lost to follow-up. All survivors (n = 340) were studied from June 2004 to December 2004 (closing interval).
Survivors underwent clinical examination, an electrocardiogram, and echocardiogram every 3 months. The patients' clinical course, need for cardiac medications, and late complications were monitored. The outcome based on NYHA class was then merged to form two groups: "good" functional status (class I/II, n = 320) or "poor" functional status (class III/IV, n = 20).
Transthoracic two-dimensional, color-flow Doppler echocardiography was performed; and mitral, tricuspid, superior vena cava, hepatic vein, and pulmonary venous flow velocities were measured. Mitral or tricuspid regurgitation was assessed semiquantitatively as grade 1+ to 4+. Ejection fraction was calculated with a modification of the method of Quinones and colleagues [5]. A constrictive pattern was defined as 25% or greater increase in mitral E-velocity with respiration, and an augmented (25% or more) diastolic flow reversal in the hepatic vein after the onset of expiration compared with the inspiration phase [5].
Two hundred twenty patients (64.7%) consented to postoperative cardiac catheterization. This was performed to fulfill the study criteria in 200 patients at closing interval and to evaluate the postoperative hemodynamics in 20 patients experiencing recurrent NYHA III/IV symptoms. Correlation between the systemic venous pressures and postoperative outcome was possible in the early postoperative phase when the pressure data were available by invasive lines and in patients undergoing cardiac catheterization late postoperatively (Table 2).
Statistical Analysis
Data were analyzed with SPSS 10.0 statistical package (SPSS, Chicago, Illinois). Continuous and interval-related data are presented as the mean ± SD, whereas categorical variables are presented as frequency distribution and percentages. Qualitative data were analyzed by using the
2 test or Student's t test.
Mortality rates were calculated depending on the total number of years of follow-up for each patient. Actuarial estimates were calculated using the Kaplan-Meier technique and the log-rank test was performed to analyze statistically the difference of survival between patients undergoing total versus partial pericardiectomy. A probability value of 0.05 or less was considered statistically significant.
Baseline predictors of hospital mortality were identified by univariate cox proportional hazards analysis initially performed on candidate variables (including surgical approach as a potential explanatory variable; Table 3). Multivariate cox regression analysis was performed on the feasible independent variables (Table 4).
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Late Mortality and Morbidity
There were 18 late deaths (4.9%) due to progressive congestive heart failure (n = 5), ventricular arrhythmias (n = 4), pleuropulmonary disease (n = 5), and noncardiac illness (recrudescent neoplastic disease, n = 4).
Follow-up was 98% complete (340 of 347; range, 1 month to 20 years), and yielded 6,086 patient-years of data with a mean follow-up time of 17.9 years (SE ± 0.3; 95% confidence interval [CI]: 17.3 to 18.6). The actuarial survival at 17.9 ± 0.3 years was 83.8% ± 0.04% in group I, and 73.9% ± 0.06% in group II (p = 0.004; Fig. 2). At their last follow-up, 96.3% (286 of 297) survivors of group I and 79.1% (34 of 43) survivors of group II were in NYHA class I/II (p < 0.001). The time taken for normalization to class I/II in groups I and II was 34 ± 12 and 70 ± 22 days, respectively (p < 0.001).
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Ascites, low ejection fraction (0.40 or less), hyperbilirubinemia, renal dysfunction, higher preoperative right atrial pressure (greater than 24 mm Hg), hyperbilirubinemia, renal dysfunction, atrial fibrillation, pericardial calcification, tricuspid and mitral regurgitation, partial pericardiectomy, thoracotomy approach, and postoperative low-output syndrome were significant negative factors for survival according to univariate analysis (Table 3).
Multivariate analysis identified only seven predictors for death after pericardiectomy (Table 4). The risk of death was 4.5 times higher (95% CI: 2.05 to 9.75) in patients undergoing partial pericardiectomy as compared with total pericardiectomy.
| Comment |
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The role of corticosteroids in the management of tuberculous pericarditis is controversial [79]. Despite steroid treatment, 150 of 156 patients (96.1%) had features of constriction, and 42 patients had effusive-constrictive pericarditis with chest pain and inability to be weaned from steroids. Thus, corticosteroids were not helpful in the prevention of constriction in our patients. Presently, in patients with significant pericardial effusion, our policy is to drain the effusion using a pigtail catheter and plan for an early pericardiectomy.
The diagnosis of constrictive pericarditis remains a challenge and is achieved by echocardiography, computed tomography, magnetic resonance imaging, and cardiac catheterization [49]. The association of characteristic hemodynamic changes with pericardial thickness greater than 3 mm is usually confirmatory [49].
Surgical Approach
Reports addressing the issue of surgical approach, the extent of pericardiectomy, and postoperative hemodynamics are limited and controversial [15]. In this series, thoracotomy was the preferred approach in the setting of purulent pericarditis and effusive-constrictive pericarditis. The literature does not specifically address the choice of surgical approach in the setting of bacterial pericarditis. Thoracotomy was the preferred option in the subset of patients because of the presence of concomitant pyothorax and the concerns of sternal infection. It was possible to achieve total pericardiectomy in these patients because of loculations and poorly formed fibrinous adhesions. Patients undergoing emergency pericardiectomy have been included in the analysis because of inadequate pericardiocentesis and the development of early signs of constriction.
In the present study, of 383 patients with pericardial thickening greater than 3 mm, 57 (14.9%) underwent partial paricardiectomy through thoracotomy, and 326 patients (85.1%) underwent total pericardiectomy through sternotomy. Median sternotomy provided good exposure of the right atrium and the venae cavae and enabled excellent clearance of the diseased pericardium. Wherever the constricting peel was very adherent and calcified, we left behind islands of pericardium. In the event of inadvertent excessive bleeding (n = 7), the patient could easily be connected to CPB. There was normalization of intracardiac pressures after total pericardiectomy within 24 hours in the great majority of patients (89.6%) of group I. The degree of reduction of filling pressure was significantly different between the groups (p < 0.001).
Cardiopulmonary Bypass During Pericardiectomy
Elective and routine utilization of CPB during pericardiectomy was recommended by Copeland and associates [10]. Surgical accidents are prone to occur because fibrous invasion of the myocardium and to the thin-walled atria. We used CPB in cases of inadvertent excessive bleeding in only seven patients. Our results indicate that CPB is not a necessary adjunct for "total" pericardiectomy and should be employed only in special circumstances.
Tuberculous Versus Nontuberculous Etiology and Total Versus Partial Pericardiectomy
Our mortality rate (7.6%) compares favorably with the 6% to 19% in-hospital mortality rate of large series published after 1985 [49]. Unlike others, there was no effect of age or tuberculous etiology on late survival presumably because of our young patient population, and timely institution of chemotherapy and surgery [49]. Analysis of the published series substantiates advanced NYHA symptoms as the most common risk factor for death [310]. In our study, data analyses did not reveal the effect of NYHA class on survival. This would be related to the predominance of NYHA class III and IV (98.2%) and the lack of death among class II patients. Constrictive epicardial sclerosis has been incriminated as a causative factor of delayed recovery or persistent hemodynamic abnormalities after pericardiectomy [2, 3, 7]. In our experience, multivariate analysis demonstrated 4.5 times higher risk of death after partial pericardiectomy as compared with total pericardiectomy. Sudden death has been reported in the setting of constrictive pericarditis and after pericardiectomy [4, 6, 9]. In this series, cardiac-related late death were due to progressive congestive heart failure in 5 patients and ventricular arrhythmias in 4 patients.
Our study demonstrates that total pericardiectomy is associated with decreased operative mortality (p = 0.02), less postoperative low-output syndrome (p < 0.001), abbreviated hospitalization (p < 0.001), and better long-term survival than partial pericardiectomy (p = 0.004; Figs 1 and 2). Even after the perioperative period, the survival rate was superior in patients undergoing total pericardial resection (297 of 306 [97%] versus 43 of 52 [82.7%]; p = 0.001) at a mean follow-up time of 17.9 ± 0.3 years.
The total pericardiectomy group achieved NYHA I and II status quicker than the partial pericardiectomy group (p < 0.001; Table 2). Normalization of cardiac hemodynamics in patients undergoing total pericardiectomy may be the possible reason for shorter interval to attain NYHA I/II status. It is noteworthy that 9 of 43 partial pericardiectomy survivors (20.9%) and 11 of 297 total pericardiectomy survivors (3.7%) experienced recurrent NYHA class III to IV symptoms during follow-up. Recurrent constriction after incomplete pericardiectomy might be the causative factor in the partial pericardiectomy group. The culprit pathophysiologic mechanisms responsible for recurrent congestive heart failure among the total pericardiectomy survivors are not well characterized. Diastolic filling characteristics remained abnormal in this subset of patients.
Results of this study and a review of published reports indicate that regardless of the operative approach or the extent of pericardial resection, a subset of patients with constrictive pericarditis will develop low-output syndrome after pericardiectomy [26]. In this study, despite total pericardiectomy, 6 patients had early postoperative deaths due to low-output syndrome. Autopsy findings have documented evidence of myocardial fibrosis and atrophy in these patients. Poor results, with persistent elevation of ventricular filling pressures, have been variously attributed to inadequate decortication, fibrous invasion of the myocardium, atrophy of myocardial fibers, "remodeling" of the ventricles, worsening tricuspid regurgitation, and postoperative mitral regurgitation secondary to papillary muscle elongation [26, 1114].
Reoperations for recurrent constrictive pericarditis after partial pericardiectomy are common [11]. Published reports attest to the unpredictable and variable pattern of constrictive pericarditis and lend support to thorough and radical decortication [3, 10, 11]. In the present series, 9 patients who underwent partial pericardiectomy in other institutions required reoperation for recurrent symptoms, and 1 died of low cardiac output in the immediate postoperative period.
Study Limitations
Ideally, the comparison of the two techniques should be limited to tuberculosis patients. Since thoracotomy was the preferred option in patients with purulent pericarditis, inclusion of purulent pericarditis among other etiologies may be an important bias in this study.
We conclude that total pericardiectomy is associated with lower mortality, less postoperative low-output syndrome, early normalization of hymodynamics, and better long-term survival compared with partial pericardiectomy. In patients with constrictive pericarditis, this is more easily accomplished through median sternotomy. Routine use of CPB during pericardiectomy is not necessary. Tuberculous and nontuberculous etiologies are nonpredictors of operative survival.
| Acknowledgments |
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