Precautions When Performing Pericardiocentesis in Patients with Cardiac Tamponade-complicated Malignancy: A Case Report and Review of the Literature

Abstract

A 51-year-old woman who had previously undergone left mastectomy for left breast cancer accompanied by multiple metastasis experienced worsening dyspnea. Physical and imaging assessments of the hemodynamics suggested cardiac tamponade, and emergency pericardiocentesis was successfully performed. However, immediately after the procedure, the patient's condition deteriorated rapidly and showed pulseless electrical activity. Contrast-enhanced computed tomography with continuous mechanical support demonstrated massive thrombi in both pulmonary arteries. An abrupt decrease in the central venous pressure and an increase in the venous return following pericardiocentesis might result in the migration of a deep venous thrombus and fatal acute pulmonary thromboembolism.

Introduction

The definitive treatment of cardiac tamponade includes the removal of pericardial fluid, which relieves elevated intrapericardial pressure and improves the hemodynamic status (1). Percutaneous pericardiocentesis can be safely and effectively performed under echocardiographic guidance. The incidence of major complications following percutaneous pericardiocentesis by experienced professionals ranges from 1.2% to 1.6% (2-5). The most serious but rare complications are lacerations or perforations of the myocardium and coronary vessels (6). In addition, patients may experience air embolism, pneumothorax, arrhythmias (usually vasovagal bradycardia), and puncture of the peritoneal cavity or the abdominal viscera. Internal mammary artery fistulas, acute pulmonary edema, and purulent pericarditis are rarely reported (6). Complications that are not generally recognized may arise following pericardiocentesis in patients with cardiac tamponade concomitant with a hypercoagulable state, including malignant diseases (7-10).

We herein report a patient with malignancy who experienced pulmonary thromboembolism (PTE)-related rapid hemodynamic deterioration occurring immediately after pericardiocentesis for cardiac tamponade. We also performed a literature review regarding PTE-related rapid hemodynamic deterioration following pericardiocentesis.

Case Report

A 51-year-old woman with a complaint of worsening dyspnea over the past week was urgently admitted to our hospital. She had been diagnosed with left breast cancer accompanied by bone and lung metastasis at 47 years old. She underwent left mastectomy followed by radiation and chemotherapy (cancer stage: IIA and pathological diagnosis of invasive ductal carcinoma). At 50 years old, the cancer metastasized to the right hilar lymph nodes, mediastinal lymph nodes, bone, and lung; therefore, she was continued on chemotherapy (Tegafur/Gimeracil/Oteracil; TS-1^Ⓡ). Her Khorana score before chemotherapy had been 1, corresponding to an intermediate risk for venous thromboembolism (VTE) (11). Her familial and personal medical histories were unremarkable except for breast cancer with multiple metastases.

Contrast-enhanced computed tomography (CT) performed 23 days prior to admission revealed neither pericardial nor pleural effusion (Fig. 1A). Thrombi were not observed in either the pulmonary arteries or deep veins of the lower extremities. Chest radiography and plain CT performed four days prior to admission showed newly appearing bilateral pleural and pericardial effusions (Figure 1B, 2A, B). The patient underwent right thoracentesis, which enabled drainage of 450 mL of exudative pleural fluid.

Figure 1.

Images of computed tomography. (A) Twenty-three days prior to admission for cardiac tamponade. No thrombi were observed in either the pulmonary arteries or deep veins of the lower extremities. No pericardial or pleural effusion was observed. (B) Four days prior to admission. A large amount of pericardial and bilateral pleural effusion was observed. (C) After pericardiocentesis. The patient was intubated, and percutaneous cardiopulmonary support was initiated. Massive thrombi were observed in the bilateral pulmonary arteries (white arrows). In addition, there was a small thrombus in the left popliteal vein (yellow arrow).

Figure 2.

Chest X-ray findings. (A) Approximately one month prior to admission. Neither enlargement of the mediastinum nor bilateral pleural effusion was observed. (B) Four days prior to admission. Enlargement of the mediastinum and bilateral pleural effusion were observed (black arrow). Therefore, drainage of 450 mL of exudative right pleural fluid was performed through right thoracentesis. (C) On admission. Right-side dominant bilateral pleural effusion was observed despite drainage of the right thoracic cavity four days prior (black arrows). Further enlargement of the mediastinum was also observed (white arrows).

A physical examination on admission revealed a blood pressure of 95/70 mmHg, heart rate of 120 beats/min (regular rhythm), respiratory rate of 25 breaths/min, and oxygen saturation (SpO₂) of 93% (room air). An invasive arterial pressure line revealed pulsus paradoxus of >10 mmHg. Respiratory sounds were attenuated in the bilateral lower lung fields. Heart sounds diminished in intensity, without murmurs, rubs, or gallops. Bilateral leg edema without laterality or redness was observed; however, her jugular vein could not be adequately evaluated due to her obesity (body mass index of 36.4 kg/m²). The laboratory examination results are shown in Table 1. A chest radiograph demonstrated right-side dominant bilateral pleural effusion, despite drainage of the right thoracic cavity four days prior to admission (Fig. 2C). The mediastinum was enlarged, which was suggestive of pericardial effusion. An electrocardiogram (ECG) on admission showed sinus tachycardia and a newly appeared low-voltage QRS complex in the broad limb and precordial leads (Fig. 3A, B). Echocardiography also showed circumferential and massive pericardial effusion (Fig. 4A). The right ventricle (RV) was collapsed to a slight extent, and the inferior vena cava (IVC) was markedly dilated without respiratory variation. The peak tricuspid regurgitant velocity (TRV) was 3.56 m/s, corresponding to a pressure gradient of 51 mmHg (Fig. 4B).

Table 1.

Laboratory Findings on Admission.

Hematology

Blood chemistry

WBC

10,600

/μL

TP

6.7

g/dL

UA

9.5

mg/dL

Neutrophils

75.4

%

Alb

3.5

g/dL

Na

129

mEq/L

RBC

345

×104/μL

AST

127

U/L

K

4.9

mEq/L

Hb

12.2

g/dL

ALT

110

U/L

Cl

95

mEq/L

Ht

35.7

%

LDH

365

U/L

Ca

9.1

mg/dL

Plt

15.5

×104/μL

γ-GTP

75

U/L

Mg

2.0

mg/dL

T-bil

3.0

mg/dL

CRP

3.21

mg/dL

Coagulation

D-bil

0.7

mg/dL

PT-INR

1.94

CK

3

U/L

Endocrinology

APTT

30.0

s

CK-MB

<4

U/L

BNP

60.1

pg/mL

Fibrinogen

176

mg/dL

Troponin I

38.8

pg/mL

D-dimer

9.09

μg/mL

BUN

17

mg/dL

AT-III

76

%

Cr

0.81

mg/dL

Alb: albumin, ALT: alanine aminotransferase, APTT: activated partial thromboplastin time, AST: aspartate aminotransferase, AT-III: antithrombin-III, BNP: brain natriuretic peptide, BUN: blood urea nitrogen, Ca: calcium ion, CK: creatine kinase, CK-MB: creatine kinase myocardial band, Cl: chloride ion, Cr: creatinine, CRP: C-reactive protein, D-bil: direct bilirubin, γ-GTP: gamma-glutamyl transpeptidase, Hb: hemoglobin, Ht: hematocrit, K: potassium ion, LDH: lactate dehydrogenase, Mg: magnesium ion, Na: natrium ion, Plt: platelet, PT-INR: prothrombin time-international normalized ratio, RBC: red blood cell, T-bil: total bilirubin, TP: total protein, UA: uric acid, WBC: white blood cell

Figure 3.

Electrocardiogram findings. (A) Before the development of cardiac tamponade. No abnormality was observed. (B) On admission due to cardiac tamponade. Sinus tachycardia and low voltages in the broad limb and precordial leads were observed. (C) Immediately after pericardiocentesis. Right-axis deviation and an incomplete right bundle branch block appeared newly.

Figure 4.

Echocardiogram findings before pericardiocentesis. (A) Apical four-chamber image. A large amount of pericardial effusion was observed. The right ventricle was slightly collapsed. (B) Tricuspid regurgitant jet velocity measured by continuous Doppler imaging. The peak tricuspid regurgitant velocity was 3.56 m/s, corresponding to a pressure gradient of 51 mmHg.

Physical and imaging findings suggested cardiac tamponade with hemodynamic instability. Therefore, we attempted emergent pericardiocentesis under echocardiographic guidance, in which 320 mL of bloody pericardial fluid was slowly and successfully removed using a syringe. However, immediately after the pericardiocentesis, the patient's condition rapidly deteriorated. She complained of dyspnea, and her systolic blood pressure and SpO₂ decreased to 60 mmHg and 50%, respectively, followed by pulseless electrical activity (PEA). Full resuscitation, including percutaneous cardiopulmonary support (PCPS), was initiated. The ECG showed a newly appearing right-axis deviation and an incomplete right bundle branch block (Fig. 3C). Based on the time course and ECG findings, we suspected an acute PTE.

Contrast-enhanced CT was performed with continuous PCPS support, which detected massive thrombi in both pulmonary arteries (Fig. 1C). A small thrombus was also observed in the dilated left popliteal vein. Therefore, PTE and deep venous thrombosis (DVT) were the definitive diagnoses. Despite resuscitative efforts, including balloon pulmonary angioplasty, the patient succumbed, and autopsy was not performed. An analysis of the aspirated pericardial fluid revealed adenocarcinoma, suggesting that metastasis of the pericardium resulting from the underlying breast cancer had been the cause of the pericardial effusion and cardiac tamponade.

Discussion

In the current case report, we describe a patient with malignancy-induced cardiac tamponade who experienced PTE-related rapid hemodynamic deterioration immediately after pericardiocentesis. Malignant diseases are often associated with cardiovascular diseases and are collectively known as “onco-cardiology” (12-14). Both cardiac tamponade and PTE are important sequelae of malignancy (6,15). PTE-related rapid hemodynamic deterioration is usually not anticipated while performing pericardiocentesis. Therefore, our case report highlights the importance of considering these complications when performing pericardiocentesis in patients with malignancy.

The most common and potent risk factor for VTE is an active malignant disease, which accounts for approximately 20% of VTE incidence (16). Malignancy activates the coagulation system and induces a hypercoagulable state (15). Clinical factors associated with increased cancer-associated VTE include cancer-, patient-, and treatment-related factors (13,14). The pathological type of adenocarcinoma and its advanced stage, female sex, obesity, low performance status, and continued chemotherapy were relevant factors in the present case. Notably, rapid progression of cardiac tamponade might cause venous stasis and also lead to VTE (Fig. 5). Virchow's triad consists of all these components (17).

Figure 5.

Possible underlying pathogenesis of concurrent cardiac tamponade and venous thromboembolism in patients with malignancy.

The etiology of pericardial effusion varies in previously published reports, with malignancy rates ranging from 13% to 39% (18-22). Pericardiocentesis is indicated for cardiac tamponade or when a bacterial or neoplastic etiology is suspected to be the cause of pericardial effusion (1). In our case, neither pericardial effusion nor VTE was evident on previous contrast-enhanced CT images until 23 days prior to admission, indicating rapid disease progression.

Previous reports have suggested two possible mechanisms that account for the rapid PTE-related hemodynamic deterioration following pericardiocentesis. One mechanism is that the abrupt increase in venous return following the removal of pericardial effusion fluid resulted in migration of the deep venous thrombus and fatal acute PTE (Mechanism A) (Fig. 6A) (7). Warsame et al. reported that a patient developed PEA immediately after successful pericardiocentesis (7). During resuscitation, an echocardiogram confirmed that the mobile thrombus had moved back and forth between the right atrium (RA) and RV through the tricuspid valve and rapidly disappeared into the pulmonary artery. The other mechanism is that drainage of pericardial effusion caused an imbalance between the intrapericardial and RV pressure (Mechanism B) (Fig. 6B) (8). The increased intrapericardial pressure through cardiac tamponade augmented RV contraction in the setting of PTE, outweighing the negative impact on RV filling. After draining the pericardial effusion fluid and increasing RV filling, the RV lost the assistance of the pericardial cavity and could not withstand the high afterload caused by PTE, thus leading to collapse. Both cardiac tamponade and PTE can cause obstructive shock. However, paradoxically, the increased right heart pressure due to PTE may have a protective effect on the tamponade physiology (9). In our case, we did not evaluate VTE immediately before pericardiocentesis; therefore, the mechanism responsible is unclear. However, an ECG carried out immediately after the collapse showed typical findings of acute PTE; hence, we assumed that newly developed acute PTE following pericardiocentesis (Mechanism A) was the cause of the rapid hemodynamic deterioration. Through a PubMed search, we found five English articles describing PTE-related rapid hemodynamic deterioration following pericardiocentesis published from 1970 to 2022 (Table 2) (7-10,23). Four cases were associated with malignancy (7-10). Regarding the cause of hemodynamic deterioration, mechanisms A and B were identified in cases 1 and 2, respectively (7,8); however, the relevant mechanisms in the remaining three cases were undetermined (9,10,23).

Figure 6.

Possible underlying pathogenesis. (A) Newly developed pulmonary thromboembolism following pericardiocentesis (Mechanism A). (B) Manifestation of right ventricular dysfunction due to coexisting pulmonary thromboembolism (Mechanism B). PTE: pulmonary thromboembolism, CVP: central venous pressure, DVT: deep venous thrombosis, RV: right ventricle

Table 2.

Reported Cases of Patients Who Experienced Pulmonary Thromboembolism-related Rapid Hemodynamic Deterioration Following Pericardiocentesis.

Case	Age (years), Sex	Reference	Underlying disease	Suggested mechanism of hemodynamic deterioration following pericardiocentesis	In-hospital outcome
1	84, M	(7)	Esophageal cancer	A: Newly developed pulmonary thromboembolism following pericardiocentesis	Death
2	87, M	(8)	Cancer of unknown primary	B: Manifestation of right ventricular dysfunction due to coexisting pulmonary thromboembolism	Alive
3	48, F	(10)	Lung cancer	Undetermined whether mechanism A or B	Death
4	75, F	(23)	None	Undetermined whether mechanism A or B	Alive
5	72, F	(9)	Breast cancer	Undetermined whether mechanism A or B	Alive

The coexistence of cardiac tamponade and PTE may be underestimated because the presence of cardiac tamponade makes a PTE diagnosis challenging (24); both induce right-sided heart failure symptoms, including dyspnea, fatigue, tachycardia, hypotension, and jugular vein distention. In patients with acute PTE, the increase in the RV systolic pressure usually causes RA and RV dilatation. In contrast, in patients with cardiac tamponade, collapse of the RA at end-diastole and RV in early diastole is usually observed due to elevated intrapericardial pressure. Because cardiac tamponade and PTE have opposing effects on the RA and RV, when complicated by cardiac tamponade, typical echocardiographic findings of PTE are masked, making the diagnosis difficult. In our case, in addition to the rapid increase in pericardial effusion, mild collapse of the right-sided heart and dilatation of the IVC were observed. Therefore, we diagnosed the patient with cardiac tamponade. However, the peak TRV was elevated to 3.56 m/s (51 mmHg of pressure gradient) before the pericardiocentesis, suggesting that PTE had already developed and coexisted with the cardiac tamponade.

When considering pericardiocentesis in patients with malignancy, concomitant VTE due to hypercoagulability induced by malignancy should be considered. Prior D-dimer testing and an evaluation of the swelling of the lower extremities should be carried out. In patients with a high suspicion of VTE, when the hemodynamics are relatively stable, imaging studies prior to pericardiocentesis, including CT pulmonary angiography or Doppler lower-extremity ultrasound, are necessary and useful for proper risk stratification. When a high-risk thrombus is detected in the IVC or proximal deep veins of the lower extremities, a vena cava filter may be a preventive option. In patients with PTE/VTE, anticoagulation therapy is the first-line treatment option, and routine use of an IVC filter is not recommended (25). However, IVC filters should be considered when anticoagulation is contraindicated. Patients with malignancy are sometimes contraindicated for anticoagulation treatment. In particular, anticoagulation immediately before pericardiocentesis may contribute to bleeding risk.

Conclusion

Pericardiocentesis in patients with malignant conditions complicated by cardiac tamponade may lead to the development of acute PTE or worsening of PTE physiology. Physicians should consider the coexistence of VTE in these clinical scenarios.

The authors state that they have no Conflict of Interest (COI).

Manabu Nitta and Keiko Takano contributed equally and are the first authors.