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(Chest. 2002;122:893-899.)
© 2002 American College of Chest Physicians

Technical and Prognostic Outcomes of Double-Balloon Pericardiotomy for Large Malignancy-Related Pericardial Effusions*

Huang-Joe Wang, MD; Kwan-Lih Hsu, MD, PhD; Fu-Tien Chiang, MD, PhD; Chuen-Den Tseng, MD, PhD; Yung-Zu Tseng, MD and Chiau-Suong Liau, MD

* From the Cardiology Section, Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan.

Correspondence to: Kwan-Lih Hsu, MD, PhD, Cardiology Section, Department of Internal Medicine, National Taiwan University Hospital, No 7, Chung-Shan South Rd, Taipei, 100, Taiwan; e-mail: klhsu{at}ha.mc.ntu.edu.tw


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Objective: To investigate both the use of immediate or elective double-balloon pericardiotomy (DBP) in patients with a large amount of malignancy-related pericardial effusion, and the prognosis of this subgroup.

Design: Observational study after DBP intervention.

Setting: Tertiary referral center.

Patients and interventions: Fifty patients with malignancy, mainly lung and breast cancer, who were admitted to our critical care unit with a large amount of pericardial effusion. All received echocardiographic-guided pericardiocentesis. Group 1 consisted of 12 patients (24%) who received immediate DBP, and group 2 consisted of 38 patients (76%) who received delayed DBP 2.5 ± 1.7 days later (mean ± SD) after emergency pericardiocentesis with pigtail catheter drainage.

Measurements: After the procedure, and at 1 month, 3 months, and 6 months, echocardiography and chest radiography were performed to check for pneumothorax, pericardial effusion reaccumulation, or the appearance of pleural effusion after pigtail catheter removal.

Main results: The procedure was successful and without recurrence in 44 patients (88%). Procedural complications were fever in 4 patients (33%) and 10 patients (26%) in group 1 and group 2, respectively (p = 0.72), and mild pneumothorax in 2 patients (17%) and 1 patient (3%) in group 1 and group 2, respectively (p = 0.14). Fifty percent of the patients died within 4 months, while 25% survived to 11 months. High serum calcium, a low albumin/globulin ratio, and positive results on pericardial effusion cytology were poor prognostic factors for long-term survival.

Conclusion: Both immediate and delayed DBP are a safe and effective method of relieving large pericardial effusions in patients with cancer. Successful DBP without recurrence of pericardial effusion was achieved in 88% of all patients. Survival was related to the extent of the disease.

Key Words: cancer • cardiac tamponade • percutaneous balloon pericardiotomy • pericardial effusion • pericardiocentesis


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Patients with large malignant pericardial effusions are often in a symptomatic, preterminal stage. Previous reports1 2 3 have demonstrated the poor prognosis of this population, and that the survival of this subgroup is most closely related to the extent of disease and the tumor type. In addition, it has been reported that pericardial lesions are the direct or contributory cause of death in 86% of untreated patients with symptomatic malignant pericardial effusion.4 Frequently, life-threatening cardiac tamponade occurs in those patients, and requires the immediate removal of the pericardial fluid to reverse the hemodynamic instability. Previously reported approaches to the effective control of new-onset or recurrent malignant pericardial effusion consist of repeated pericardiocentesis, external beam radiation, the instillation of sclerosing or chemotherapeutic agents, subxiphoid surgical windowing, and pericardiectomy.5 6 7 8 9 10 Nevertheless, cancerous cachexia, in conjunction with a shortened life-expectancy, portend a poor candidate for general anesthesia and surgical intervention.

In 1991, Palacios and coworkers11 first reported the usefulness of single-balloon percutaneous balloon pericardiotomy (PBP) in the management of eight patients with malignant pericardial effusion. This favorable experience was supported by a multicenter registry that collected data from 130 patients undergoing PBP from 1987 to 1994 in 16 centers.12 The technical modification of PBP included dilatation at two adjacent pericardial sites, the use of an Inoue balloon catheter, and the double-balloon technique.13 14 15 In this study, we report the first large series of patients in whom the double-balloon technique was used to treat large amounts of pericardial effusion in a subgroup with advanced malignancy. Our aim was twofold: first, to examine the feasibility of using the immediate or delayed double-balloon technique following pericardiocentesis; second, to refine the prognostic factors of this subgroup.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Study Patients
Fifty patients with malignant pericardial effusion underwent double-balloon pericardiotomy (DBP) between January 8, 1997, and November 8, 2000, at National Taiwan University Hospital. The individual malignancy types are listed in Table 1 . Lung cancer and breast cancer accounted for 40 of the patients (80%). Pericardiocentesis for malignant pericardial effusion had been performed in 6 patients (12%) before. After informed consent was obtained, all patients underwent emergency pericardiocentesis with echocardiographic guidance. Twelve patients (24%) who received immediate DBP following pericardiocentesis were placed in group 1. Thirty-eight patients (76%) who underwent pigtail catheter drainage after pericardiocentesis, followed by delayed DBP 2.5 ± 1.7 days later (mean ± SD), were placed in group 2. DBP was approached via either the precordium or the subxiphoid, depending on which showed the wider pericardial space on the echocardiogram. A large amount of pericardial effusion was defined as pericardial effusion >= 2 cm in depth in any of the echocardiographic views. Cardiac tamponade was defined as a paradoxical pulse pressure > 10 mm Hg and/or the presence of echocardiographic tamponade signs (right ventricle collapse in the early diastole or the right atrium collapse over one third of the cardiac cycle). Forty-one patients (82%) had cardiac tamponade develop. The pericardial effusion was sent for examinations of biochemistry measurements, cell count, cytology, and culture for nontuberculous bacteria, tubercle bacilli, and fungi. Thirty-five patients died from their malignancy during the follow-up period.


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  		Table 1.. Tumor Types Found in the 50 Patients

 
Technique Description
Pericardiocentesis was performed with an 18-gauge puncture needle, and a 7F sheath was placed in the pericardial cavity. If direct DBP was performed subsequently, two 0.035-inch, 150 cm-long J-tip guidewires were advanced through the same sheath. Then the sheath was removed and replaced by two sheaths along each of the two guidewires. Thereafter, an 8- to 12-mm by 2-cm balloon (Meditech; Boston Scientific Cooperation; Watertown, MA), and an 8- to 12-mm by 4-cm balloon (Smash; Schneider; Bülach, Switzerland) were advanced into the pericardial cavity through each guidewire. The size of the balloons was largely dependent on the body habitus of the patient. If the patient’s body habitus was smaller, smaller balloons were used to create an adequate pericardial window without undue damage to the subcutaneous tissue. The guidewires separated from each other after they had passed the subcutaneous tissue and entered the relatively free space of the pericardial cavity. Under fluoroscopy, this nearest or crossover point between the two guidewires could be easily identified, indicating the pericardial border. Both balloons were partially inflated, and their locations were adjusted to place the balloon centers just at the pericardial border. The two balloons were inflated simultaneously until their waists disappeared (Fig 1 ). Then the longer balloon was held still, while the shorter one was pushed and pulled across the pericardium several times to ensure the creation of an adequate pericardial window, opening into the pleural cavity. Both balloons were then removed, and a 6F pigtail catheter was indwelled in the pericardial cavity for the complete drainage of the effusion. Before the DBP procedure, 50 mg of meperidine was injected IM to alleviate discomfort.



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  		Figure 1.. Top, A: Two guidewires in the same tract separate from each other after their entrance into the pericardial cavity, so that the pericardial border can be defined clearly under fluoroscopy. Middle, B: Double balloons were straddled over the pericardium. Both balloons were partially inflated and showed a central waist appearance. Bottom, C: Fully expanded double balloons creating a pericardial window.

 
Postprocedure Management and Follow-up
After the procedure, the pigtail catheter was connected to a suction bottle. If daily drainage was < 100 mL for 2 days, the pigtail catheter was removed. Echocardiography and chest radiography were performed to check for pneumothorax, the possible reaccumulation of pericardial effusion, or the appearance of pleural effusion draining through the pericardial window after pigtail catheter removal. These examinations were also performed at 1 month, 3 months, and 6 months. Procedure failure was defined as an inability to complete the DBP due to technical problems or the recurrence of pericardial effusion requiring drainage. A requirement for thoracentesis due to new-onset or increased left pleural effusion within 30 days was considered to be the result of successful pericardiotomy.

Statistical Analysis
Statistical analyses were performed using software (Version 10.0 for Windows; SPSS; Chicago, IL). Continuous variables were reported as mean ± SD. A {chi}2 test and an unpaired t test were used to determine the significance of difference between the proportion and mean values, respectively. Two-sided p values were reported.

The survival data of the entire malignancy-related large pericardial effusion cohort were computed using a Cox regression model. The factors adjusted included age; sex; presence of cardiac tamponade; immediate or delayed DBP; values of serum calcium, lactic dehydrogenase, and hemoglobin; platelet count; albumin/globulin (A/G) ratio; time lag from the diagnosis of malignancy to the DBP; DBP procedure success; amount of drained pericardial effusion before removal of the pigtail catheter; results of the cytology of the pericardial effusion; and primary malignancy cell type.

Odds ratios and their 95% confidence intervals were calculated. The Kaplan-Meier survival curve was used to characterize the timing of mortality during the follow-up period, with a comparison done for the separate groups using the log-rank test. In all stepwise procedures, a variable was allowed to enter into the model if it reached a significant contribution at the 0.05 level, and it was removed if it could not reach a contribution at the 0.10 level after the subsequent addition of other variables.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
Clinical Characteristics
As shown in Table 2 , there was no significant difference in the demographic profiles and serum biochemistry measurements between patients undergoing immediate DBP (group 1) and delayed DBP (group 2). The only two clinical variables showing a significant difference were the presence of cardiac tamponade, and the presence of adenocarcinoma; both were lower in group 1 (p < 0.001 and p = 0.046, respectively). Adenocarcinoma was frequent in both groups (58% in group 1 and 87% in group 2), probably indicating its invasive biobehavior. The positive rate of pericardial effusion cytology for malignancy was 67% in group 1 and 87% in 2 (p = 0.34). This suggests that the underlying malignancy was in an advanced stage in most patients.


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  		Table 2.. Clinical Characteristics of the 50 Patients*

 
Procedure Results
As shown in Table 3 , DBP procedure characteristics showed no difference between the two groups. DBP was mostly approached from the precordium. The amount of drained pericardial effusion in both groups was 618 ± 479 mL and 797 ± 64 mL, respectively (p = 0.18). The postprocedure removal of the pigtail catheter was at 2.9 ± 0.8 days later in group 1, and 4.0 ± 3.5 days later in group 2 (p = 0.08).


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  		Table 3.. Procedural Characteristics of the 50 Patients*

 
Follow-up Findings
As shown in Table 4 , the mean follow-up period was 134 ± 164 days in group 1 and 142 ± 139 days in group 2 (p = 0.86). Successful DBP without the recurrence of pericardial effusion was achieved in 88% of all patients (92% vs 87% in group 1 and group 2, respectively; p = 1.0). Six patients had a procedure failure. One failure was due to a breakage of the balloon, which remained in the pericardial space while it was being pulled across the pericardium in the inflated state. Retrieval of the broken fragment using a snare was tried but was unsuccessful. It was then removed during surgical pericardiotomy. The other five patients had a symptomatic moderate-to-large amount of pericardial effusion develop once again, and so underwent further DBP or surgical procedures. The mean intervals of recurrence were 16 days and 27 ± 18 days in groups 1 and 2, respectively (p = 0.61). Fever developed in 33% of group 1 patients and in 26% of group 2 patients (p = 0.72). However, most of them had fever before the procedure. Mild pneumothorax without the need of drainage occurred in three patients. In the follow- up period, 25% of the patients in group 1 received a left-side pleurocentesis, compared with 27% in group 2 (p = 0.72).


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  		Table 4.. Follow-up Results for the 50 Patients*

 
Analysis of Prognostic Factors
The survival curve of the entire malignancy- related large pericardial effusion cohort is presented in Figure 2 , top, A. Fifty percent of the patients died within 4 months, while 25% survived to 11 months. Cox regression revealed that a positive pericardial effusion cytology result, high serum calcium level, and a low A/G ratio conferred a negative influence on long-term survival (Table 5 ). Figure 2 , bottom, B shows the adjusted survival curve in relation to the results of the cytology of the pericardial effusion (log-rank p = 0.0159).



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  		Figure 2.. Top, A: Proportional survival of patients with malignancy-related large pericardial effusions: 50% of the patients died within 4 months after they underwent balloon pericardiotomy; 25% survived after 11 months. Bottom, B: Adjusted survival curve constructed by a Cox regression model revealed that a positive cytology result for pericardial effusion is a poor prognostic factor (p = 0.0159).

 

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  		Table 5.. Prognostic Factor Analysis

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
This report is the first study to describe the feasibility and efficacy of DBP. It confirms the previous good results of the single-balloon technique.12 16 In cancerous patients with symptomatic large pericardial effusion, the standard treatment has consisted of pericardiocentesis and drainage.17 The recurrence rate after pericardiocentesis may be as high as 62%.5 Recurrence suggests the need for repeated hospitalization, with its attendant cost, morbidity, and mortality. Therefore, primary therapy with a pericardial window creation should be considered. This was our aim, resulting in an 88% success rate after the first DBP.

The timing for DBP is dependent on both hemodynamics and logical considerations. Most of our patients had cardiac tamponade develop and warranted immediate relief of their pericardial effusion. So pericardiocentesis was done first to relieve the hemodynamic instability. DBP followed immediately, if the facilities of the cardiac catheterization laboratory were available at that time. Otherwise, the DBP could be arranged for a later date. In addition, some patients were referred from other departments or hospitals after diagnostic or therapeutic pericardiocentesis. This also delayed the performance of DBP. Both immediate and delayed DBP can be safely performed, as demonstrated by the similar prognosis and complications of the two groups. Our recommendation is that DBP can be performed in an immediate or delayed situation if the cardiac tamponade is relieved successfully by the preceding pericardiocentesis. The timing of DBP depends on the discretion of the individual operator.

The ideal procedure for patients with malignant pericardial effusion should ensure a low recurrence and minimum discomfort. Surgical subxiphoid pericardial windowing has been proposed as a treatment of choice because of its higher success and lower recurrence rates.10 18 19 However, the procedure entails a 8- to 10-cm vertical incision over the xiphoid process and upper abdomen, which is followed by dividing the linea alba and freeing the xiphoid process. After the creation of a 2- to 3-cm pericardial window, a 26F chest tube needs to be placed under the heart and brought out through a separate wound.20 This procedure is much more invasive than the DBP using two 7F sheaths through one small incision, and increases the patient’s discomfort and risk of secondary infections. Besides, a 1.2% mortality rate has been reported with the use of subxiphoid pericardiotomy.2 A more extensive total pericardiectomy or pericardial resection via an anterior thoracotomy requires general anesthesia, with a mortality rate as high as 13.3%2 and morbidity up to 67%.10 No deaths have occurred in our experience or the experience of others2 12 performing balloon pericardiotomy. Two patients in our group underwent repeated DBP without a recurrence of pericardial effusion until they died of the underlying malignancy. It might be reasonable to conclude that DBP, being less invasive, could be performed repeatedly without detriment to patient survival or quality of life.

Ziskind et al16 reported that 2 of their 50 patients could not be dilated with a single large balloon due to the resistance of the pericardium. Iaffaldano et al14 also reported that in two patients, during single-balloon inflation, the oval profile of the balloon easily slipped from its position straddled in the pericardial border into the less-resistant pericardial space. All of the above-mentioned four cases were treated successfully with the double-balloon technique. Two simultaneously inflated balloons lying adjacent to each other can achieve a stronger tension, are more rectangular in shape compared to the single, large inflated balloon, and tend to be more securely located in the pericardial border. We therefore conducted consecutive performances of DBP in all malignancy patients with a large amount of pericardial effusion. All were successful, except for one procedure failure due to a fracture of the balloon catheter in the pericardial space as the balloon was being pulled out in an inflated state.

The double-balloon technique has additional advantages. Two guidewires in the same tract separate or cross over each other after their entrance into the pericardial cavity, so that the spatial definition of the pericardial border can be defined clearly under fluoroscopy. Furthermore, one short and one long balloon were used due to mechanical considerations. The inflated long balloon could be partially fixed across the pericardium. The inflated short balloon then utilized this long balloon as an anchoring rail to move in and out several times across the pericardial border to ensure an adequate opening of the window. This was able to greatly reduce subcutaneous tissue damage. In contrast, a single larger balloon created more extensive subcutaneous damage, and increased patient discomfort and the possibility of pneumothorax, as illustrated by the Inoue balloon. This larger-profile balloon could be located at the pericardial border due to its special design. However, its proximal bell might straddle or even be outside of the chest wall, and cause chest wall laceration and pneumothorax.15

Tsang et al21 examined 275 patients with malignancy- related pericardial effusion and noted that a positive fluid cytology for malignancy was associated with a poor prognosis. Wiener et al22 had the same finding. Similarly, a positive pericardial effusion cytology result was an important prognostic factor in our study, after adjustment for other variables. Since a positive cytology finding implies a more disseminated state of the underlying cancer, further treatment to enhance survival is indicated in such a subgroup.

Park et al10 utilized multivariate analysis in his malignancy patients and noted that the time period from diagnosis of malignancy to surgery, and the serum level of lactic dehydrogenase, could adversely affect the prognosis. Our data did not reveal a similar relationship. Instead, after an adjustment was done on 14 separate variables, the importance of a high calcium and low A/G ratio to a poor prognosis was clearly shown. These two variables were not included in the study by Park et al.10

High serum calcium in malignancy might suggest a tumor more disseminated to the skeletal system, or a humoral effect. The selection of the A/G ratio as our adjustment factor, instead of albumin and globulin separately, was based on the correlated property of both factors. In spite of the fact that albumin and globulin appeared significant in our preliminary prognostic factor analysis, their significance levels were lower than that of the A/G ratio. So the latter was chosen, without missing the clinical implication. Phillips et al23 reported the association of low albumin and high mortality in different diseases, including cancer. Darne et al24 noted that a high globulin level negated survival. Both studies acknowledged the importance of serum proteins to mortality. The inflammatory state of terminal cancer leads to the production of many cytokines, including interleukin-1, interleukin-6, and tumor necrosis factor, and these cytokines can modulate the shift of protein synthesis from albumin to another acute phase protein, so that albumin decreases.25 26 A positive cytology finding of pericardial effusion and an abnormal serum biochemistry result represent an extensive involvement and the disseminated nature of terminal cancer.

This retrospective study enrolled patients with large amounts of pericardial effusion, mostly with attendant cardiac tamponade. The relatively small population size may have allowed some other significant prognostic factors to remain undetected. Since no patient had severe coagulopathy in this study, we still do not known whether or not this approach can be performed safely with that type of patient.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
Both immediate and delayed DBP are safe and effective methods for helping cancer patients with large amounts of pericardial effusion. The 12% recurrence rate of all patients makes it the treatment of choice in this population. Survival was poorer among patients with more disseminated cancer.


   Footnotes
 
Abbreviations: A/G = albumin/globulin; DBP = double-balloon pericardiotomy; PBP = percutaneous balloon pericardiotomy

Received for publication September 17, 2001. Accepted for publication February 28, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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