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10.1245/s10434-006-9073-1
Annals of Surgical Oncology 13:1732-1738 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Surgical Management of Symptomatic Pericardial Effusion in Patients with Solid Malignancies

Jefferson Luiz Gross, MD, PhD1, Riad Naim Younes, MD, PhD1, Daniel Deheinzelin, MD, PhD1, Alessandro Landskron Diniz, MD2, Rodrigo Afonso da Silva, MD1 and Fabio José Haddad, MD, PhD1

1 Department of Thoracic Surgery, Hospital do Cancer A. C. Camargo, Rua Professor Antonio Prudente, 211 Liberdade, São Paulo, SP 01509-010, Brazil
2 Department of Surgery, Hospital do Cancer A. C. Camargo, Rua Professor Antonio Prudente, 211 Liberdade, São Paulo, SP 01509-010, Brazil

Correspondence: Address correspondence and reprint requests to: Jefferson Luiz Gross, MD, PhD; E-mail: jefluizgross{at}yahoo.com.br


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Symptomatic pericardial effusion in patients with cancer may lead to a life-threatening event that requires diligent treatment, but the best surgical treatment is still controversial. The purpose of this study was to identify predictors of survival for patients with solid malignancies and symptomatic pericardial effusion, which might help to select the best surgical treatment for each patient.

Methods: We retrospectively analyzed 47 patients with solid malignancies concomitant with symptomatic pericardial effusion who underwent surgery between 1994 and 2004. Overall survival was calculated from date of surgery, and prognostic importance of clinical and pathological variables was assessed.

Results: The most common primary sites of disease were breast (46.8%) and lung (25.6%). Initial pericardiocentesis were performed in 29 patients; median volume of fluid drained was 480 mL. Median interval from the diagnosis of primary cancer to the development of pericardial effusion (pericardial effusion-free interval) was 34.8 months. Definitive surgical treatment was performed in 43 patients, as follows: subxiphoid pericardial window (n = 21); thoracotomy and pleuropericardial window (n = 10); pericardiodesis (n = 8); and videothoracoscopic pleuropericardial window (n = 4). Pericardiocentesis was the only procedure in four patients. Median follow-up was 2.9 months. Median overall survival was 3.7 months. Pericardial effusion-free interval longer than 35 months and more than 480 mL of fluid drained at initial pericardiocentesis were determinants of better survival.

Conclusions: Pericardial window and pericardiodesis seem to be safe and efficacious in treating effusion of the pericardium. Pericardial effusion-free interval and volume drained at initial pericardiocentesis are determinants of outcome.

Key Words: Malignancy • Pericardium • Surgery • Prognosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although symptomatic pericardial effusion is uncommon in patients with cancer, autopsy studies show involvement of the pericardium by malignancies in 1% to 20%. The most common primary sites are lung, breast, and lymphoma.1,2 Despite being less frequently observed than malignant pleural effusion, symptomatic fluid collection within the pericardium may lead to cardiac tamponade, a potentially life-threatening event that requires diligent treatment. The pathophysiology of fluid accumulation includes metastatic spread to the pericardium, direct pericardial invasion by adjacent thoracic tumors, mediastinal malignant disease, or previous mediastinal radiotherapy that may cause pericardial effusion by means of disruption of normal lymphatic mediastinal drainage.3

Treatment of pericardial effusion in patients with cancer must address two issues: relief of acute symptoms and hemodynamic effects of cardiac tamponade; and prevention of fluid reaccumulation within the pericardium. Patients with malignant pericardial effusion generally have widespread disease refractory to systemic and radiation treatment, which limits the effectiveness of these therapies in promptly relieving symptoms, as required by this life-threatening complication. It is often necessary to drain pericardial effusion before proceeding with specific treatment of the primary cancer.4 Pericardiocentesis, a less invasive procedure performed under local anesthesia, is effective as an acute means to relieve symptoms. However, most patients develop fluid re-accumulation shortly after fluid drainage.5 Pericardial window by means of subxiphoid approach, or pleuropericardial window through thoracotomy or video-assisted thoracoscopy are both effective methods for controlling acute symptoms and result in a low rate of recurrence. On the other hand, they have the disadvantage of being a more invasive approach, with general anesthesia required in severely ill patients.6,7 A procedure, pericardiocentesis and intrapericardial sclerosis, was described recently and appears to be a less invasive procedure with good rates of control of pericardial effusion.8 Other, more aggressive approaches, such as pericardiectomy, are rarely indicated for the treatment of patients with advanced malignant disease.9 The best treatment of pericardial effusion is still controversial because there are no definitive, prospective, comparative trials addressing this issue.

Selecting which patients should be considered for each type of treatment for pericardial effusion presents a challenge for oncologists. The search of prognostic factors for patients with symptomatic pericardial effusions that require treatment may help clinicians to decide how aggressive they should be treating these life-threatening events in patients with cancer.

The purpose of this study was to examine predictors of survival in patients with solid malignant tumors and symptomatic pericardial effusion treated surgically at a single institution.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From October 1994 to October 2004, we reviewed the records of patients with symptomatic pericardial effusion and solid malignant tumors in a tertiary cancer-care center. All patients were submitted to surgical treatment for pericardial effusion at Department of Thoracic Surgery, Hospital do Cancer A. C. Camargo, São Paulo, Brazil. Inclusion criteria were as follows: histological diagnosis of solid malignant disease before or concomitant with the development of pericardial effusion; diagnosis of pericardial effusion confirmed by echocardiography or ultrasonography; presence of symptoms attributed to pericardial effusion; and surgical treatment of pericardial effusion.

Patients developed pericardial effusion during or after the primary diagnosis of cancer at any site, but all patients had active malignant disease at the time of pericardial effusion. The diagnosis of pericardial effusion was considered according to radiological criteria (echocardiography and/or ultrasonography), and the time between the diagnosis of primary malignancy and pericardial effusion was established as the pericardial effusion-free interval. All patients had symptoms attributed to pericardial effusion, but cardiac tamponade was defined by clinical (tachycardia, hypotension, and signs of jugular venous distension) or echocardiographic findings confirming tamponade, as reported by the radiologist. We considered oncologic treatment (chemotherapy or radiotherapy) concomitant to pericardial effusion when it was in course at the time of the diagnosis of symptomatic pericardial effusion.

Initial pericardiocentesis (Marphan technique) for diagnosis and symptom relief was defined as the procedure performed before the definitive surgical treatment of pericardial effusion. Definitive surgical treatment was classified as follows: pericardiocentesis, pericardial window, or pericardiodesis. All pericardial windows were performed in the operating room with patients under general anesthesia. Three different types of pericardial window were performed: subxiphoid pericardial window; anterolateral thoracotomy with pleuropericardial window; and video-assisted thoracoscopy and pleuropericardial window. Pericardiodesis was performed by inserting a double lumen catheter in the pericardial space (Seldinger technique), followed by intrapericardial sclerotherapy with thiotepa (15 mg diluted in 50 mL of normal saline solution), under local anesthesia. The type of surgical treatment was performed according to the surgeon’s preference.

Because this is a retrospective study, no rigid protocol had been established to follow these patients after the surgical procedure. Each surgeon established the follow-up routine individually. Complications of operative procedures and recurrence of pericardial effusion data were recorded. Recurrence was defined as a reaccumulation of symptomatic pericardial fluid, confirmed by echocardiography, and requiring medical intervention.

Overall survival was calculated from date of surgical procedure to treat pericardial effusion. The Kaplan-Meier test10 was performed to estimate survival, and differences were calculated by log rank test. Multivariate analysis of prognostic factors was not performed because too few patients were included in the study.

Prognostic significance of the following clinical variables was assessed: age, sex, Karnofsky performance status index, site of the primary malignancy, pericardial effusion-free interval, volume of fluid drained at first pericardiocentesis, oncologic treatment at time of symptomatic pericardial effusion, malignant pleural effusion associated to pericardial effusion, echocardiographic findings of cardiac tamponade, positive cytologic malignancy in the pericardial fluid, or metastasis in the pericardial biopsy sample. All statistical analyses were performed with SPSS 10.0 software. P < .05 was defined as statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
During the 10-year period from 1994 to 2004, a total of 48 patients diagnosed with pericardial effusion and malignancies at any site were identified in a retrospective review of the records of all patients treated at our service. One patient who received a diagnosis of lymphoma was excluded from the analysis. There were 16 men and 31 women; median age was 52.6 years (range, 15–79 years). The median Karnofsky performance status index at the time of diagnosis was 70% (range, 50%–90%). Other clinical characteristics of the patients are listed in Table 1Go.


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  		TABLE 1. Clinical characteristics of 47 patients
 
The most frequent clinical manifestation was dyspnea (46 patients), followed by jugular stasis (n = 15), distant heart sound (n = 15), and arrhythmia (n = 5). Concomitant malignant diseases were present in all patients. The primary sites were breast (46.8%), lung (non–small cell cancer) (25.6%), thymoma (6.4%), stomach (4.2%), kidney (2.1%), larynx (2.1%), colon (2.1%), ovary (2.1%), uterine cervix (2.1%), thyroid (2.1%), and unknown (4.2%). Median interval from the diagnosis of the primary malignancy to the diagnosis of symptomatic pericardial effusion was 34.8 months (range, 0–151 months). Pericardial effusion-free interval longer than 35 months was observed in 22 patients, and from these patients, most (68.2%) had breast cancer as the primary site.

Pleural effusion was frequently observed in association with pericardial effusion (n = 41, 87.2%). However, in 20 patients (42.5%), malignant cells were observed in the pleural effusion. Before definitive surgical treatment, pericardiocentesis was performed in 29 patients (61.7%). The median volume of fluid drained at initial pericardiocentesis was 480 mL (range, 60–1000 mL). The aspect of pericardial effusion was grossly bloody in most patients (n = 23, 79.3%). Of the 47 patients included in this study, pericardial effusion was confirmed to be malignant in 30 patients (63.8%), according to cytologic or pathologic findings.

Definitive surgical treatment was performed in 43 patients (91.5%); pericardiocentesis was the only treatment in the remaining 4 patients. These four patients died of cancer 1 day, 15 days, 2 months, and 14 months after pericardiocentesis, respectively. The patient with the longest survival (14 months) after the isolated procedure had presented with breast cancer that was being treated with systemic chemotherapy for advanced disease. The other patients had advanced lung cancer (n = 2) and breast cancer (n = 1). The different types of surgical procedures performed are listed in Table 2Go. Length of postoperative stay ranged from 1 to 23 days (median, 4 days); there was one intraoperative death due to myocardial rupture in a patient submitted to subxiphoid pericardial window. This rupture was a consequence of a digital exploration maneuver for loculated pericardial effusion. This patient had his right ventricle myocardium invaded by a friable pericardial mass. Postoperative morbidity rate was 6.4%. Two patients had arrhythmia, and respiratory failure was observed in one patient. Only one patient, who was submitted to pericardiodesis, had recurrence of symptomatic pericardial effusion 54 days after the procedure, and this patient was successfully treated by subsequent subxiphoid pericardial window.


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  		TABLE 2. Surgical procedures performed to treat pericardial effusion
 
Median follow-up of all patients was 2.9 months (range, 0–25.2 months). At the time of last follow-up, 14 patients (29.8%) were still alive without evidence of pericardial effusion, 32 patients (68.1%) had died of cancer, and 1 patient died from another cause (pulmonary thromboembolism 1 day after pericardiocentesis). Median overall survival was 3.7 months. Overall, pericardial effusion-free interval was determinant of prognosis. Patients with more than 35 months of pericardial effusion-free interval had better overall survival (Fig. 1Go). From 29 patients who underwent initial pericardiocentesis, the volume drained at this procedure was associated with prognosis. Patients with drained volume of less than 480 mL had the worst overall survival (P = .03) (Fig. 2Go). Median overall survival of patients with pericardial effusion and breast cancer was better (5.2 months) than other primary malignancies (3.2 months); however, this difference did not reach statistical significance (P = .53). Patients submitted to pericardiodesis (n = 8) had shorter survival time (2.5 months) than patients treated by pericardial window (n = 35, 4.6 months). This difference was also not statistically significant (P = .32). Sex, age, Karnofsky performance status index, presence of cardiac tamponade, associated malignant pleural effusion, concomitant chemotherapy, and pathologic or cytologic confirmation of malignant pericardial effusion did not greatly affect prognosis in this series of patients.


Figure 1
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  		FIG. 1. Overall survival according to interval of time between diagnosis of primary cancer and development of pericardial effusion. Solid line >35 months (n = 25); dashed line ≤35 months (n = 22) (P < .01, log rank test).

 

Figure 2
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  		FIG. 2. Impact of volume of pericardial fluid drained at first pericardiocentesis on overall survival. Solid line >480 mL (n = 15); dashed line ≤480 mL (n = 14) (P = .03, log rank test).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Pericardial effusion in patients with cancer occurs less frequently than malignant pleural effusion. However, it is often an acute, life-threatening event. At our institution, a tertiary cancer-care center, in a 10-year period, we identified only 47 patients requiring surgical treatment for symptomatic pericardial effusion associated to solid tumors from several primary sites. The largest similar series of patients included 63 patients in an 11-year period; 17 of these patients (27%) had hematologic malignancies.11 Similarly, Girard et al.12 described 60 patients in an 11-year period, where 11 patients (18.3%) had hematologic malignancies. Neoplasms most frequently associated with pericardial effusions are breast cancer, lung cancer, hematologic malignancies, and melanoma.2,11 These data are in agreement with our results, where 72.4% of pericardial effusions were associated with breast and lung cancer. We decided to exclude one patient with hematologic malignancy because of the patient’s high response rate to systemic and radiation therapies, which might overestimate the success rate of surgical treatment of pericardial effusion.4

The development of symptomatic pericardial effusion is commonly associated with advanced cancer, so these patients characteristically have short-term survival,13,14 as observed at the present study (median, 3.7 months). Pericardial effusion may occur at any time in the clinical course of cancer. Despite this, few authors reported the interval from the diagnosis of primary malignant disease to the development of pericardial effusion.15,16 In the present study, we observed that pericardial effusion can be detected at the time of the primary diagnosis of malignant disease, or may develop as late as 151 months after the initial diagnosis of primary cancer. The median interval to the development of pericardial effusion was 34.8 months, and breast cancer was the most common malignancy associated with late presentation of pericardial effusion.

Concurrent pleural and pericardial effusions are commonly observed because both are markers of advanced disease.3 In the present study, most patients (87.2%) had pleural effusion diagnosed concomitant to pericardial effusion. However, only 42.5% had malignant cells confirmed in the pleural fluid. Similar results were reported by Wang et al.,16 who described 90% of pleural effusion concurrent to pericardial effusion, but only 41% of malignant pleural effusion among 82 patients with non–small cell lung cancer. On the basis of these data, one might suppose that the presence of pleural effusion can be a consequence of cardiac failure due to pericardium effusion, and the concomitant neoplasmic involvement of pleura as commonly observed in advanced malignant disease.

Although chemotherapy and radiotherapy may be options for patients who present with mild symptoms, in the present series, these therapeutic approaches were not performed as an exclusive treatment because all patients had symptoms caused by fluid accumulation within the pericardium. Such finding is in accordance with previous studies that concluded that radio and chemotherapy are less effective than any invasive approach to treat these patients.17

In the present study, 29 patients (61.7%) were submitted to pericardiocentesis as the initial approach to symptomatic pericardial effusion. The median volume of pericardial fluid drained at this procedure was 480 mL. That is sufficient to cause cardiac tamponade, as described by Spodick.18 In our series, from these 29 patients submitted to initial pericardiocentesis, only 4 patients did not undergo definitive surgical treatment. Pericardiocentesis can be performed as an emergency life-saving procedure, but as the sole treatment, it is associated with a high rate of pericardial effusion re-accumulation (>90%), requiring further definitive treatment unless the underlying causes can be corrected.19 Because malignant pericardial effusions are usually associated with advanced disease, response to chemotherapy or radiotherapy is not promptly expected. Accordingly, pericardiocentesis alone can relieve symptoms, but it is not usually effective as the definitive treatment of symptomatic malignant pericardial effusion.4,20 Moreover, it is seldom adequate for long-term palliation.

Intrapericardial instillation of sclerosing agents is an option to treat malignant pericardial effusion.21–25 The main objective of pericardiodesis is to prevent the recurrence of pericardium effusion, and the efficacy of this method to control malignant pericardial effusion ranges from 70% to 90%, according to different series.3,4 In the present study, only eight patients were submitted to pericardiodesis with thiotepa. One patient had arrhythmia after pericardiodesis, and another patient had recurrence of pericardial effusion requiring subxiphoid pericardial window 54 days after pericardiodesis. There was no difference in overall survival between patients submitted to pericardiodesis and pericardial window. Although there were few patients in the pericardiodesis group and definitive conclusions comparing these two procedures cannot be drawn in the present study, these results are in accordance with previously published data.12

Pericardial window is the most common procedure to treat malignant pericardial effusion, although there is no agreement about the best method to perform it.11 In the present study, most of our patients (74.5%) were submitted to a surgical pericardial window as the definitive treatment, and subxiphoid was the most common access (44.7%), followed by thoracotomy (21.3%) and thoracoscopy (8.5%). Pericardiectomy was not performed in our series. From these patients, we observed a low morbidity (6.4%), and only one patient (2.1%) died of myocardial rupture during a subxiphoid pericardial window approach. It is difficult to compare outcomes between different surgical methods to create a pericardial window because of the marked heterogeneity of patients and approaches in the present study, as has been observed in the retrospective series of others.11

Recently, less invasive techniques for surgical treatment of pericardial effusion have been described, such as percutaneous balloon pericardiotomy.26,27 However, this approach should be compared with other surgical procedures before definitive conclusions can be drawn. This procedure was not performed in the patients included in the present study.

As a life-threatening event, malignant pericardial effusion requires treatment, and the search of factors predictive of survival might help the clinician choose which treatment should be presented to the patients to consider. Patients with poor prognosis should receive less invasive treatment; but on the other hand, patients with a longer life expectancy might be treated more aggressively. In the present study, the interval between diagnosis of primary malignancy and development of symptomatic pericardial effusion determined prognosis; a longer interval (more than 35 months) was associated with far better survival. We believe that shorter interval to development of pericardial effusion might be associated with more aggressive malignant disease. Park et al.5 reported that time from diagnosis of malignancy to surgical treatment of pericardial effusion determined survival only at multivariate analysis of 28 patients with cancer; however, the authors did not specify the amount of time between primary diagnosis and surgery for pericardial effusion. Most of our patients were submitted to an initial pericardiocentesis before definitive surgical treatment of pericardial effusion. We observed that the volume of fluid drained at this pericardiocentesis was determinant of survival; patients with >480 mL of fluid drained at pericardiocentesis had better survival than patients with ≤480 mL of fluid drained. To our knowledge, similar results have not been described before, and we believe that lower volume of fluid in pericardium determines symptoms because of its rapid rate of accumulation, and it might be associated with more aggressive cancer. The impact of fluid volume accumulation in the serous cavity was previously assessed by Haddad et al.28 in patients with malignant pleural effusion; the authors observed that greater volume of pleural effusion was associated with adverse results of pleurodesis.

We conclude that symptomatic pericardial effusion in patients with cancer is associated with a dismal prognosis, but as a life-threatening event, it should be treated. There is no agreement about the best method to treat these patients with advanced malignant disease, because most of the published series are retrospective and heterogeneous. Surgically created pericardial window seems to be a safe and efficacious method of treatment; however, it almost always requires general anesthesia in patients with poor performance status. Pericardiodesis has been described as a safe, efficacious, and less invasive procedure than pericardial window, although there are no prospective, randomized trials comparing these two methods of treatment. Our study disclosed two variables associated with prognosis in patients with symptomatic pericardial effusion and solid malignancy. The prognostic importance of the interval from diagnosis of primary malignancy to development of pericardial effusion was better defined. The volume of fluid drained at first pericardiocentesis was described for the first time as being a determinant of outcome in these severely ill patients who undergo surgical treatment of pericardial effusion. The knowledge of both variables might help in the decision-making process when we decide how invasive we should be in treating pericardial effusion in patients with cancer.

Received for publication February 8, 2006. Accepted for publication May 19, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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