A preliminary study on contrast characteristics and clinical application of bedside transthoracic contrast-enhanced ultrasound in iatrogenic cardiac tamponade

Introduction

Iatrogenic cardiac injury refers to heart damage caused by medical treatments or interventions. This condition includes issues such as acute myocardial infarction, arrhythmias, heart failure, and pericardial tamponade. Pericardial tamponade is a serious complication with an incidence rate of 0.7–6% (1-5). It is often induced by cardiac perforation (6) during interventional procedures using catheters and guidewires. New technologies and complex surgeries have increased the risk of pericardial effusion and tamponade in patients (5,7,8).

The pericardium normally helps to maintain blood volume, but if fluid accumulates rapidly (even as little as 50 mL), hemodynamic decompensation can occur (9). This impairs left ventricular function, potentially leading to shock or cardiac arrest (10). Therefore, the timely diagnosis and treatment of iatrogenic cardiac tamponade (ICT) are crucial.

Currently, the diagnosis of ICT relies on clinical symptoms, electrocardiogram (ECG), chest X-ray, and echocardiography (11). However, these approaches have significant limitations in quickly and accurately locating hemorrhage sites (12). Contrast enhanced ultrasound (CEUS) offers real-time, portable, and safe imaging, showing higher accuracy in diagnosing ICT by locating bleeding points and assessing volume, guiding timely treatment.

However, research on bedside CEUS in ICT is extremely limited, with only single-center case reports (13-15). This study retrospectively analyzed 84 patients’ data and outcomes, including CEUS findings and myocardial contrast echocardiography (MCE) parameters in 29 patients. We evaluated how these parameters and contrast model in predicting ICT prognosis. This study also introduces an innovative classification system for pericardial tamponade imaging with bedside CEUS. Our goal is to establish a stronger evidence base for the selection and optimization of treatment strategies for patients. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-aw-2371/rc).

Methods

Clinical data

This retrospective study analyzed 84 patients with iatrogenic pericardial effusion treated at Fuzhou University Affiliated Provincial Hospital between March 2018 and December 2024. The cohort included 29 patients who underwent bedside CEUS (CEUS group) and 55 patients who did not undergo CEUS evaluation (control group). The patient selection process is illustrated in Figure 1. Baseline clinical data, including gender, age, symptoms, family history, personal history, and relevant medical history, were extracted from the medical record system. Our retrospective study was approved by the Human Ethics Review Committee of Fuzhou University Affiliated Provincial Hospital (No. K2025-08-008). This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. All patients provided written informed consent prior to the CEUS examination as part of routine clinical care; however, the requirement for informed consent specifically for this retrospective study inclusion was waived by the Human Ethics Review Committee of Fuzhou University Affiliated Provincial Hospital because the research involved only a review of existing medical records and maintained patient confidentiality.

Figure 1 Flow chart of patient enrolment and selection criteria for the study.

The inclusion criteria were as follows: (I) patients who developed iatrogenic pericardial effusion/cardiac perforation secondary to interventional or surgical procedures; (II) clinical presentation consistent with pericardial tamponade; (III) provision of informed consent for CEUS by the patient or their legally authorized representative; and (IV) availability of complete ultrasound images and clinical data.

The exclusion criteria were as follows: (I) patients with pericardial effusion attributable to non-iatrogenic causes such as infectious causes (e.g., tuberculosis), malignancy, or autoimmune disorders; (II) incomplete ultrasound images or clinical data; and (III) refusal to undergo CEUS.

Conventional echocardiography

All patients underwent conventional echocardiography using a phased-array transducer (frequency: 3.5 MHz; Mindray, Shenzhen, China). Patients were positioned in the left lateral decubitus position and instructed to maintain steady breathing. Synchronized epicardial electrocardiographic leads were connected to ensure accurate cardiac cycle assessment. The following parameters were systematically evaluated and recorded: (I) cardiac dimensions: left atrial diameter (LAD), left ventricular end-diastolic diameter (LVD), right atrial diameter (RAD), right ventricular diameter (RVD), left ventricular posterior wall thickness, left ventricular volume, and pulmonary artery pressure; (II) cardiac function: left ventricular ejection fraction (LVEF); (III) wall motion score: regional wall motion abnormalities were assessed and scored according to standard protocols; (IV) pericardial effusion volume: effusions were categorized as moderate or large based on established criteria. All conventional echocardiographic images were acquired and interpreted by experienced cardiac sonographers with more than 5 years of clinical expertise.

CEUS examination

Patients suspected of having ICT based on clinical symptoms or initial conventional echocardiography were evaluated for CEUS. The decision to perform CEUS was made by the attending interventionalist in consultation with a senior sonographer. In this study, all patients with confirmed ICT underwent emergency pericardiocentesis and pericardial drainage as the primary intervention. After obtaining the patient consent, CEUS was performed using a portable ultrasound system (Mindray, Andover, MA, USA) with a 3.5 MHz phased-array transducer and synchronized epicardial electrocardiographic leads were connected to ensure precise cardiac cycle timing. A bolus of 1.0 mL of SonoVue (Bracco, Italy) was injected via the median cubital vein, followed by a 3–5 mL saline flush. Active real-time contrast-enhanced imaging mode with ultra-low mechanical index (MI, MI <0.2) was used to achieve optimal visualization of the rupture site and the entire heart. In this mode, we first identified the rupture location and degree of contrast agent concentration, observing the varying contrast effects as the agent leaks through the rupture. Subsequently, MCE mode was activated at end-systole of the left ventricle with MI <0.3, slowly infusing contrast agent at 1 mL/min. Between 5–10 frames, the “Flash” key and the high MI (MI =1.3) ultrasound impulse we employed to rupture microbubbles and clear them from the microcirculation. Dynamic images were acquired in the apical three-chamber, four-chamber, and two-chamber views, including imaging results of the rupture site before and after flash and normal myocardium, 5 cardiac cycles before the flash, and 15 cardiac cycles after the flash. The CEUS imaging protocols and administration of contrast agents in our study were performed in strict accordance with the standardized cardiac exam recommendations provided by the International Contrast Ultrasound Society (16).

The examinations were performed by two experienced cardiac sonographers with over 10 years of clinical practice with emergency protocols in place to manage potential adverse reactions. The criteria and technical protocols for CEUS remained consistent to ensure the reliability and reproducibility of the imaging data.

Quality control and image analysis

To ensure the accuracy and reliability of the imaging data, stringent quality control measures were implemented throughout the study. Operators were required to systematically acquire cardiac images in strict accordance with standardized echocardiographic views. Prior to each examination, the ultrasound equipment and measurement software were tested to confirm proper functionality. Any anomalies detected during testing were addressed through repeated measurements to minimize potential errors.

Two experienced (over 10 years) cardiac radiologists independently evaluated the bedside CEUS images. In cases of disagreement, a third senior cardiac radiologist was consulted to provide an adjudication. The final classification was determined based on a majority consensus to ensure objectivity and consistency. The imaging manifestations of bedside CEUS were categorized based on the severity and characteristics of pericardial effusion as follows: (I) “Dark Night Sign”: CEUS demonstrated the absence of microbubble extravasation into the pericardial cavity, indicating no active bleeding. (II) “Falling Snow Sign”: CEUS revealed intermittent, linear extravasation of contrast microbubbles from the bleeding site into the pericardial cavity, suggesting slow or intermittent hemorrhage. (III) “Blizzard Sign”: CEUS showed aggregation of contrast microbubbles within the pericardial cavity, with directional movement of microbubbles along the cardiac rupture site, indicative of active and continuous bleeding. (IV) “Jet Sign”: CEUS demonstrated rapid filling of the pericardial cavity with contrast microbubbles, which were ejected from the cardiac rupture site in a jet-like manner, reflecting high-pressure or severe active bleeding. There is a summary figure of the CEUS classification system in Figure 2.

Figure 2 Representative contrast-enhanced ultrasound patterns of ICT. (A) “Dark Night Sign” (no extravasation): CEUS with a complete absence of microbubbles within the pericardial space (dashed lines). This visual darkness reflects a stable state with no active bleeding or a sealed rupture site. (B) “Falling Snow Sign” (slow/intermittent leak): characterized by sparse, intermittent, and linear microbubble extravasation (arrowhead). The microbubbles descend slowly within the pericardial effusion, resembling falling snow. This pattern suggests a low-flow or intermittent hemorrhage, typically from a small or partially self-sealing defect. (C) “Blizzard Sign” (active/continuous bleeding): a more intense manifestation where a dense cloud of microbubbles aggregates rapidly within the pericardial cavity. The microbubbles exhibit clear directional movement originating from the cardiac rupture site (arrowhead), indicating continuous, moderate-to-high volume active bleeding. (D) “Jet Sign” (high-pressure/massive hemorrhage): characterized by a high-velocity, focused “jet” of microbubbles (arrowhead) ejected forcefully from the rupture site. The microbubbles rapidly disperse and fill the pericardial cavity in a turbulent manner, reflecting high-pressure bleeding requiring immediate intervention. Pericardial cavity (white dashed box), bleeding point (arrowhead). CEUS, contrast-enhanced ultrasound; ICT, iatrogenic cardiac tamponade.

Further analysis of myocardial perfusion parameters was performed by Tomtec (Philips, Amsterdam, Netherlands) software. All images were independently analyzed by two senior cardiac ultrasound doctors who remained unaware of patient-specific information throughout the process. Regions of interest (ROIs) were placed on both the myocardial area adjacent to the tear (lesion part) and the normal myocardial area without tears (normal part), ensuring consistent ROIs size. Manual adjustments were made when necessary to avoid ROI placement on the pericardium or left ventricle. The ROI was required to remain in the same anatomical location during the entire contrast agent filling cycle. The software calculated parameters such as ascending slope (β), time to peak (TTP), and peak intensity (A) according to the formula: y(t)=A(1−e−βt)+C.

Prognostic evaluation

Prognostic assessment was conducted using a comprehensive approach. This included clinical symptoms, physical examination, ECG, chest X-ray, echocardiography, and laboratory tests. (I) Cure: significant clinical improvement was achieved following surgical intervention or conservative treatment. Symptoms resolved completely, and no further treatment or medical intervention was required. (II) Improvement: symptoms related to pericardial effusion were reduced. Cardiac function and laboratory parameters improved after treatment, with no evidence of disease progression. (III) Death: no clinical improvement occurred despite treatment. Symptoms worsened or the disease progressed, leading to respiratory and cardiac arrest and the cessation of brain function.

Statistical analysis

Statistical analyses were performed using the software SPSS 29.0 (IBM Corp., Armonk, NY, USA) and MedCalc version 23.1.7 (MedCalc Software, Ostend, Belgium). Normality was tested on the data. Continuous variables that followed a normal distribution were expressed as mean ± standard deviation, whereas non-normally distributed data were presented as median and interquartile range. Student’s t-tests were used to compare continuous variables between groups. Categorical variables were analyzed using the chi-square test or Fisher’s exact test. The ability of perfusion parameters was evaluated to predict prognosis in patients with ICT using receiver operating characteristic (ROC) curves. The areas under the curve (AUCs) were compared among different parameters. Intra- and inter-observer variability of perfusion parameters were assessed through the intraclass correlation coefficient (ICC). The difference was statistically significant at P<0.05.

Results

Baseline patient characteristics

A total of 84 patients with iatrogenic pericardial effusion were enrolled in this study, including 48 males and 36 females. The participants’ ages ranged from 11 to 93 years (with a mean age of 61.09±12.40 years). Among them, 29 patients who underwent CEUS were classified into the CEUS group, whereas the remaining 55 patients were assigned to the control group. As shown in Table 1, the CEUS group had a significantly higher incidence of dyspnea (65.5% vs. 36.3%) and a higher proportion of patients with a history of malignant tumors (31.0% vs. 10.9%). The differences were statistically significant (P=0.011, P=0.022). No significant differences were observed between the two groups in other characteristics (P>0.05). As summarized in Table 2, there were no significant differences between the CEUS group and the control group regarding the types of medical procedures or the anatomical sites of injury (P>0.05). The most common cause of tamponade was right ventricular perforation (44.9–47.3%), followed by catheter ablation and pacemaker-related procedures. These results indicate that the data of the patients enrolled in this study were balanced and comparable.

Results of bedside conventional echocardiography

All patients underwent bedside conventional echocardiography, and the obtained cardiac-related parameters were subjected to statistical analysis. As shown in Table 3, there were no significant differences between the two groups in terms of chamber dimensions and pulmonary artery pressure (all P>0.05). However, compared with the control group, patients in the CEUS group exhibited lower LVEF (54.17% and 56.95%, P=0.012) but overall remained within the normal range, potentially reflecting the underlying risk of cardiac dysfunction in the CEUS group. In the CEUS group, 7 patients (24.1%) presented with reduced ventricular wall motion, whereas in the control group, 13 patients (23.6%) demonstrated similar results. However, no statistically significant difference was noted. All enrolled patients presented with moderate to large pericardial effusions. The proportion of patients with large effusions was similar between the groups, with 44.8% in the CEUS group and 45.5% in the control group (P>0.05).

Results of myocardial echocardiography quantitative analysis

Myocardial perfusion analysis was performed on images from 29 CEUS patients. The statistical results in Table 4 show that perfusion parameters β, A, and A×β were significantly reduced in myocardial tissue near the tear compared to normal areas (all P<0.001). TTP was longer at the lesion site than it was in the normal areas (P=0.004).

Analysis of ROC curve

The ROC curves for myocardial perfusion parameters were further plotted to evaluate their efficacy in predicting the prognosis of patients with ICT. According to Table 5 and Figure 3, A×β demonstrated the highest diagnostic performance (AUC =0.754) with a specificity as high as 95.65%. Concurrently, ROC curve analysis revealed that β also demonstrated high diagnostic efficacy (AUC =0.750). It reached a high sensitivity for prognostic evaluation and optimal cutoff value of 4.67 dB.

Figure 3 ROC curve of MCE parameters in predicting prognosis of ICT patients. β, ascending slope; A, peak intensity; A×β, mean myocardial blood flow; ICT, iatrogenic cardiac tamponade; MCE, myocardial contrast echocardiography; ROC, receiver operating characteristic; TTP, time to peak.

Inter- and intra-observer consistency and reproducibility

The results detailed in Table 6 show that both inter- and intra-observer consistency and reproducibility of the quantitative analysis of MCE were good (P<0.001).

Comparison of treatment methods, complications, and outcomes

The treatment approaches, complications, and clinical outcomes of patients with ICT in the two groups are compared in Table 7. In the CEUS group, the rate of surgical treatment was only 17.2%, whereas that in the control group was significantly higher (40.0%, P=0.034). Complications occurred in 5 patients (17.2%) in the CEUS group, compared with 29 patients (52.7%) in the control group (P=0.002).

Regarding treatment outcomes, 23 patients and 22 patients in both the contrast group and the control group achieved complete recovery following their respective treatments (79.3% vs. 40.0%). Additionally, 1 patient (3.5%) in the contrast group and 7 patients (12.7%) in the control group died. The final clinical outcomes after treatment showed a statistically significant difference between the two groups (P=0.003). Compared to the control group, the CEUS group had a lower rate of surgery, complications, and mortality. These patients also achieved better clinical results.

Correlation between CEUS patterns and treatment strategies, complications, and outcomes

In the CEUS group, imaging findings were categorized based on specific contrast patterns. To ensure the reliability of this system, we conducted an interobserver consistency analysis. Although the sample size for individual sub-patterns is relatively small, the overall ICC of 0.95 [95% confidence interval (CI): 0.93–0.98, P<0.001] provides sufficient statistical power to demonstrate that the classification criteria are highly objective and reproducible. We subsequently correlated these imaging findings with treatment approaches, complications, and clinical outcomes. This relationship between the diagnostic data and the final patient results is illustrated in Figure 4. The results showed that patients with the “dark night sign” or “falling snow sign” predominantly underwent non-surgical treatment, with higher cure rates (86.6–100%) and lower complication rates (0–6.7%). In contrast, patients presenting with the “blizzard sign” or “jet sign” on CEUS images required surgical intervention, associated with lower cure rates (0–33.3%) and higher complication rates (50–100%). We also found that different imaging patterns demonstrated a sensitivity of 66.67% and a specificity of 95.65% in assessing patient prognosis. It is noteworthy that one patient with a jet sign had a cardiac perforation, which further explains why patients of this type have severe conditions and pose great challenges in treatment.

Figure 4 Relationship between ultrasound characteristics, treatment methods, and outcome in the CEUS group. (A) Treatment approaches for different contrast-enhanced imaging findings in ICT patients. (B) Incidence of complications associated with different contrast-enhanced imaging findings in ICT patients. (C) Prognosis for different contrast-enhanced imaging findings in ICT patients. CEUS, contrast-enhanced ultrasound; ICT, iatrogenic cardiac tamponade.

Discussion

ICT is a rapidly progressive and potentially life-threatening condition characterized by the rapid accumulation of blood within the pericardial cavity, resulting in cardiac compression and impaired diastolic function. Timely and accurate diagnosis is essential in managing this condition to prevent severe complications and improve outcomes. However, traditional imaging often fails to provide the real-time, detailed data needed for this critical choice. Our study shows that CEUS helps doctors to make faster and more accurate decisions. This approach significantly reduced the need for invasive surgery and lowered the rate of complications in our patients.

To be specific, CEUS uses unique imaging signs to guide treatment. Patterns such as the “dark night sign” and “falling snow sign” indicate slow, minimal leaking. We found that these patients usually recover well without surgery, avoiding the risks of invasive procedures. Meanwhile, the “blizzard” and “jet signs” are clear indicators of rapid, high-volume bleeding. These signs show that the patient needs immediate surgical repair. Compared to other methods, CEUS has clear advantages at the bedside. Although computed tomography (CT) offers high anatomical detail, it requires moving hemodynamically unstable patients to a radiology suite. This is often too risky for patients in shock. Furthermore, CT cannot show the dynamic, real-time process of active bleeding. Transesophageal echocardiography (TEE) is highly accurate for detecting cardiac ruptures, but it is a semi-invasive procedure. It usually requires sedation, which can further lower blood pressure and worsen the condition of a patient with tamponade. Although TEE and CT are helpful for the early diagnosis of encapsulated pericardial effusion or hematoma (17), these methods are complex and time-consuming. In contrast, bedside CEUS can not only rapidly assess the severity of the disease but also provide a scientific reference for the individualized treatment of patients with ICT.

As highlighted in the previous literature, CEUS is particularly valuable for identifying contrast agents within a pericardial effusion in critically ill patients. The presence of these microbubbles serves as a definitive indicator that active hemorrhage has not yet ceased (18). Our proposed four-pattern classification further refines this observation by categorizing the severity and dynamics of such hemorrhage. Notably, in this study, there was one patient who had been reported in our previous case (13). This involved the case of a 93-year-old patient with the “jet sign” and iatrogenic right ventricular anterior wall perforation highlights the value of CEUS in guiding minimally invasive surgical repair. Bedside CEUS enabled precise localization of the perforation site, which facilitated immediate repair via a parasternal small incision under ultrasound guidance. This approach avoided the need for a traditional thoracotomy. In Tokuda et al.’s study, 1,152 consecutive cases of catheter ablation for ventricular arrhythmias were collected, and the incidence of iatrogenic cardiac perforation and pericardial tamponade was 1.0%. The researchers suggested that patients with iatrogenic ventricular perforation require urgent surgical repair (19). In our study, we identified the location of the perforation rupture through bedside CEUS and performed bedside small incision repair under ultrasound guidance. However, the successful implementation of this small incision repair may be related to the proximity of the perforation site to the chest wall and the small size of the perforation. This case of bedside emergency repair provides a therapeutic reference for other subsequent cardiac-related emergency cases. Similarly, another patient presenting with the “blizzard sign” received thoracoscopic pericardial window surgery after CEUS-guided identification of the bleeding site. Both procedures significantly reduced surgical trauma and postoperative recovery time, with patients recovering smoothly without severe complications. Previous studies have reported the application of CEUS in identifying and ruling out cardiac rupture (20,21). Our findings further demonstrate the significant value of CEUS in locating the site of hemorrhage and guiding subsequent treatment.

Our study also provides insights into myocardial perfusion dysfunction associated with ICT. The quantitative analysis revealed significant perfusion deficits at the lesion site, and specific parameters (β and A×β) emerged as reliable predictors of patient prognosis (22). Our study shows that a β threshold below 4.67 predicts poor prognosis suggests that myocardial microcirculation impairment may serve as an early biomarker for adverse outcomes. This quantitative data adds a layer of objective risk stratification beyond subjective visual assessment, potentially guiding clinicians to adopt more aggressive treatment strategies for patients with subclinical perfusion deficits.

Despite the promising findings, this study has certain limitations. First, the retrospective design introduces inherent selection bias. Specifically, the CEUS group exhibited higher rates of dyspnea and malignancy, suggesting that these patients represented a more clinically complex or severe subset. Although we adjusted for key variables, these baseline imbalances may have influenced both treatment decisions and overall prognosis, potentially confounding the observed associations. Second, the sample size was relatively small, particularly when stratified by specific imaging patterns. These limited subgroup sizes reduce the statistical power to definitively establish the prognostic value of individual CEUS signs, which may affect the reliability of these specific correlations. Third, as a preliminary exploration, CEUS was performed immediately following emergency pericardiocentesis and drainage. The optimal time window for CEUS remains to be determined. Finally, as a single-center study, our findings are subject to institutional protocols and operator expertise. This may limit the generalizability of the results to centers with different resources or less experience in cardiac CEUS. In the future, we will continue to carry out multi-center, large-sample prospective studies to further verify our conclusions and compare CEUS findings at different time intervals post-injury to develop a more standardized, evidence-based clinical diagnostic protocol.

Conclusions

CEUS has demonstrated significant advantages in the evaluation and management of ICT. Its precision, real-time imaging capability, and bedside feasibility make it an invaluable tool for guiding individualized treatment strategies. This study introduces CEUS not only as a diagnostic modality but also as a critical component in therapeutic decision-making. By facilitating accurate localization of bleeding sites, dynamic hemorrhage assessment, and tailored treatment, CEUS significantly improves patient outcomes while reducing surgical risks and complications. Additionally, the proposed CEUS-based classification system for pericardial effusion provides an innovative framework for clinical decision-making, further highlighting the potential of CEUS as a transformative tool in the management of ICT. Future studies should focus on validating these findings and expanding the clinical applications of CEUS in emergency cardiac care.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-aw-2371/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-aw-2371/dss

Funding: This work was supported by Special Fund Project of The Second Affiliated Hospital of Fujian Medical University (grant No. 2024BD1102).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-aw-2371/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. Our retrospective study was approved by the Human Ethics Review Committee of Fuzhou University Affiliated Provincial Hospital (No. K2025-08-008) and individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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