Tricuspid annular plane systolic excursion (TAPSE) as a noninvasive echo marker in evaluating prone position effectiveness for COVID-19 patients with severe ARDS—a case series

Introduction

Background

In cases of acute respiratory distress syndrome (ARDS) resulting from primary lung damage, such as pneumonia, which accounts for 60% of cases, the alveolar air space becomes filled with fluid and inflammation, the surfactant is damaged, and the glycocalyx of the alveolar-capillary membrane is degraded. This chain of events increases pulmonary arterial compliance (CPA) and pulmonary vascular resistance (PVR), which results in pulmonary vascular dysfunction (1,2). This dysfunction causes an increase in afterload in the right heart, ultimately leading to right ventricular (RV) failure. Acute cor pulmonale (ACP) or acute right heart failure occurs due to a sudden increase in resistance to blood flow in the pulmonary circulation. This resistance may be absolute (a significant increase in PVR with normal RV contractility) or relative (a slight rise in PVR with reduced RV contractility) (3). Mechanical ventilation is necessary in cases of severe ARDS, but it can also result in ACP due to increased intrathoracic pressure. Patients with ARDS often experience respiratory and hemodynamic instability following intubation and require close monitoring of both during treatment. Using “point-of-care” ultrasound diagnostics at the bedside is a crucial safety measure for critically ill patients. Bedside echocardiography is a rapid method for diagnosing ACP (4).

Rationale and knowledge gap

The echocardiographic assessment of the right ventricle can be performed qualitatively and quantitatively using the basic echocardiographic windows, including the parasternal long and short axis and the apical and subcostal windows. A crucial aspect of treating severe ARDS is regularly alternating the patient’s position from supine to prone. With ARDS, the lungs’ relationship with the heart is a current research focus, particularly during severe respiratory illnesses like influenza or coronavirus disease 2019 (COVID-19) outbreaks. Since the lungs receive the entire cardiac output of the right ventricle, changes or disruptions in the right heart can reflect events in the pulmonary circulation. While right heart catheterisation has become the norm for hemodynamic monitoring and understanding in critically ill patients, its use in ARDS patients remains unclear. A study by Murdoch et al. has not demonstrated an increase in mortality attributable to the use of pulmonary artery catheters (PACs) but still failed to establish a beneficial effect (5). In daily critical care practice for this patient, we could use less invasive diagnostic methods such as bedside echocardiography instead of invasive pulmonary function monitoring.

Objective

Our research aimed to present tricuspid annular plane systolic excursion (TAPSE), a noninvasive ultrasound measure that tracks the function of the right heart and the effectiveness of the prone position in ARDS. Our objective is to assess the mortality risk linked to right heart failure among individuals diagnosed with ARDS. We present this article in accordance with the AME Case Series reporting checklist (available at https://jeccm.amegroups.com/article/view/10.21037/jeccm-24-117/rc).

Case presentation

Out of six hundreds patients (n=600) with severe ARDS who were treated in the intensive care unit (ICU) during the COVID-19 pandemic, only six patients (n=6) met the criteria. Inclusion criteria were that patients had an echocardiographic finding no older than 6 months that ruled out the existence of cor pulmonale or RV failure before hospitalisation for ARDS (Table 1). We measured TAPSE before the first pronation and immediately after returning the patient from the same pronation to the supine position.

Patients data

Patient 1 is a female who suffers from hypertension due to chronic diseases. She takes an angiotensin-converting enzyme (ACE) inhibitor and a beta blocker to manage her condition. At the age of 52 years, she contracted a severe form of ARDS caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pneumonia, with a Murray score of 3. After 2 days of non-invasive ventilation (NIV) with high oxygen therapy, she required invasive mechanical ventilation with analgesia (fentanyl), sedation (propofol), and muscle relaxation (atracurium). After 9 days of controlled mechanical ventilation, the patient was successfully extubated, and the ICU treatment outcome was positive. There were no thromboembolic findings on the chest computed tomography (CT) (Table 1).

Patient 2 is a male who suffers from chronic hypertension and takes an ACE inhibitor. At 55 years old, he fell seriously ill with ARDS caused by SARS-CoV-2 pneumonia (Murray score 3). Despite 2 days of NIV and high oxygen therapy, he eventually required invasive mechanical ventilation with analgosedation and muscle relaxation. After 13 days of controlled mechanical ventilation, the patient was successfully extubated and had a positive outcome from treatment in the ICU. No thromboembolic findings were detected on chest CT (Table 1).

Patient 3 is a 72-year-old male who suffers from hypertension due to chronic diseases and takes an ACE inhibitor. He fell ill with a severe form of ARDS caused by SARS-CoV-2 pneumonia (Murray score 2). During his illness, he experienced hyperglycemia, which was treated with insulin in the ICU. After 4 days of high oxygen therapy with NIV, he required invasive mechanical ventilation with analgosedation and muscle relaxation. He was under controlled mechanical ventilation for a total of 15 days, after which he was extubated, and the treatment in the ICU was successful. There were no findings of thromboembolism on chest CT (Table 1).

Patient 4 was a 66-year-old male who had hypertension as a result of chronic diseases and was taking an ACE inhibitor. He fell ill with a severe form of ARDS caused by SARS-CoV-2 pneumonia (Murray score 3). After 5 days of NIV with high oxygen therapy, he required invasive mechanical ventilation with analgesia, sedation, and muscle relaxation. A chest CT revealed segmental thromboembolism on both sides of the lungs, even before he was transferred to the ICU. Unfortunately, the patient passed away after 3 days of invasive mechanical ventilation due to cardiac arrest (Table 1).

Patient 5 was a 70-year-old female who had hypertension as a chronic disease. She used to take an ACE inhibitor and a diuretic. She had a severe form of ARDS caused by SARS-CoV-2 pneumonia (Murray score 3). She required invasive mechanical ventilation after 5 days of NIV with high oxygen therapy in the ICU, with analgosedation and muscle relaxation. The chest CT revealed a segmental pulmonary thromboembolism (PTE). Despite all the efforts, the patient passed away due to cardiac arrest after 4 days of invasive mechanical ventilation (Table 1).

Patient 6 was a 72-year-old male with hypertension caused by chronic diseases. He was taking ACE inhibitor and beta-blocker medications. ARDS caused by SARS-CoV-2 pneumonia (Murray score 3). He received NIV with high oxygen therapy for 7 days, but his condition worsened, and he required invasive mechanical ventilation with analgosedation and muscle relaxation. A chest CT revealed a segmental PTE on both sides of the lungs. The patient suffered a cardiac arrest and passed away after 7 days of invasive mechanical ventilation (Table 1).

All procedures performed in this study followed the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patients or their relatives to publish this article. A copy of the written consent is available for review by the editorial office of this journal.

Discussion

Key findings

Out of six hundreds patients (n=600) with severe ARDS who were treated in the ICU during the COVID-19 pandemic, only six patients (n=6) met the criteria. They had an echocardiographic finding no older than 6 months that ruled out the existence of cor pulmonale or RV failure before hospitalisation for ARDS.

Group S, consisting of three survivors (n=3, 50%), had the same gender composition (two men and one woman; 50% vs. 50%) as Group D, composed of three deceased (n=3, 50%). The Murray score for both groups was relatively high, ranging [mean ± standard deviation (SD)] from 2.5±0.3 for Group S to 2.8±0.3 for Group D.

The median age of Group S is lower (55 years, with a range of 20) than Group D (70 years, with a range of 6). Group S received NIV for a median of 2 days (range, 2) before being intubated. On the other hand, Group D’s respiratory weakness was treated with NIV for a longer duration, with a median of 5 days (range, 2). The length of invasive mechanical ventilation was longer in Group S by 13 days median (range, 6) until extubated, while Group D patients died after 4 days median (range, 4) from the start of invasive controlled mechanical ventilation. Despite ongoing anticoagulant therapy, all three patients from Group D (n=3, 50%) were later confirmed to have segmental pulmonary embolism based on chest CT scan findings (Table 2).

Both groups exhibited decreased TAPSE systolic mobility before pronation. Post-pronation, all patients (n=6) demonstrated RV systolic function recovery, as evidenced by increased TAPSE. Group D (n=3, 50%) showed weaker TAPSE-based RV systolic function recovery, medians 22.5 (range, 6) vs. 17.3 (range, 2) (P=0.03). Table 3 rejects the hypothesis that there is no difference between groups in that the TAPSE changes equally pre- and post-pronation.

Strengths and limitations

This observational study was conducted on a limited number of patients due to the factors that led to the exclusion of right heart cardiomyopathy in the prehospital stage. As a result, the findings and conclusions of this study should be validated on a larger sample size, preferably from multiple centres. A survey of more patients could include cardio-specific enzymes and D dimer as a measure of sensitivity and specificity compared with non-invasive echo markers and lung findings. We failed to include these parameters during the observation.

Comparison with similar research

Echocardiography can be done using a transoesophageal approach in the prone position, as suggested in the paper by Ajam and coauthors (6). However, in COVID patients, that would be questionable due to aerosol and more invasive than transthoracic echocardiography between the patients’ prone positions. Meta-analysis data on 1,430 studies screened, 51 studies reporting on 1,526 patients, were included in the study about RV dysfunction (RVD) in ARDS. Most of the studies were non-randomized experimental studies (53%), with the next most common being case reports (16%). Only 5.9% of studies were randomized controlled trials (RCTs). In total, 27% of studies were conducted to modify RV function (7). Given the prevalence of RVD in ARDS and its association with mortality, the absence of research on this topic is concerning. This review highlights the need for prospective trials to treat RV dysfunction in ARDS.

TAPSE demonstrates a strong correlation with right ventricular ejection fraction (RVEF), as assessed by radionuclide angiography, which is considered the gold standard for evaluating proper ventricular function. TAPSE is a straightforward and reliable method for measurement, providing consistent results. Its calculation, which can be multiplied by 3.2 to determine RVEF, is a valuable predictor of mortality in patients with pulmonary arterial hypertension (PAH). Notably, TAPSE depends on afterload and declines as the severity of PAH increases (8). We selected patients who underwent an echocardiography examination 6 months ago, confirming the proper functioning of the right ventricle. This helped us demonstrate that TAPSE could serve as a reliable, non-invasive indicator of changes in the right heart in COVID-19 ARDS patients. Right heart circulatory failure and severe ACP are often associated with higher driving pressure, hypercapnia, and hypoxemia. Additionally, prone positioning, positive end-expiratory pressure, and inhaled nitric oxide (INO) have been shown to provide adequate RV protection by unloading the right ventricle, improving the coupling between the pulmonary circulation and the right ventricle, and correcting circulatory failure (9). The prone position may further mitigate RV injury by enhancing venous return, reducing PVR by recruiting the lungs, reducing ventilation/perfusion mismatch, and improving gas exchange. We achieved these changes and confirmed with a reduction in TAPSE. This approach was successful in all six patients. Out of the six patients we observed, three in Group D showed a smaller TAPSE decrease than the others. This condition could be responsible for fixed dysfunctional RV weakness caused by thromboembolic obstruction of the pulmonary circulation. A consistent definition of acute RV injury in ARDS treated with invasive positive pressure ventilation is lacking, which needs to be urgently addressed (10). Echocardiographic parameters such as RV-left ventricular end-diastolic area ratio, a systolic state in the tricuspid annular plane excursion, free strain RV walls, septal kinetics and flow stroke volume index were used in some studies (11,12). Many studies favour PAC placement in critically ill patients. For example, cardiogenic shock increases the survival of these patients due to reliable diagnostic monitoring via PAC (13). However, PAC placement remains controversial in patients with ARDS. Complications from the placement of a pulmonary catheter are reported to reach around 20%. These complications encompass a wide range, including arrhythmias, misplacement, knotting, and more severe issues such as pneumothorax, arterial puncture, and direct PAC, where mortality leads to 75–100%. Additionally, there are potential risks once the catheter is in place, such as venous thrombosis, thrombophlebitis, pulmonary embolism, infarction, and valvular fatal consequences associated with pulmonary artery rupture, highlighting the critical nature of this issue (14).

In mechanically ventilated patients, performing a transthoracic echocardiogram presents a significant challenge due to air-filled lungs between the heart and the chest wall. In the intensive care setting for COVID-19, the absence of an echo probe from the start of treatment can be attributed to the high risk of aerosol generation and the burden of ensuring proper sterilization of equipment, as well as prolonged exposure to the patient’s infected particles (15,16). Despite various studies about transthoracic echocardiography in COVID-19 patients, there is still little evidence to support that the prone position positively affects RV function, as measured by noninvasive ultrasound parameters, regardless of patient outcome (17). Looking at our results, the low TAPSE values could have been influenced by the initial drop in pressure, changes in heart rhythm and myocardial kinetics dictated by opioids, anaesthetics and muscle relaxants immediately before and after intubation and starting invasive mechanical ventilation.

Explanations of findings

Based on our observations in the clinical case series, higher PVR may reduce the effectiveness of prone positioning after a minimum of 16 hours, as indicated by the TAPSE echo marker. If the TAPSE echo marker does not improve in the post-proning period, pulmonary embolism diagnostics should be considered.

Conclusions

Healthcare professionals can benefit significantly from noninvasive echocardiographic markers when diagnosing and treating patients with ARDS. One marker that can offer valuable insights into the efficacy of ARDS treatment in the prone position is TAPSE. If, even after 16 hours in the prone position, TAPSE does not show signs of improvement in the recovery of right heart systolic function, exploring the possibility of thrombosis-induced pulmonary circuit obstruction may be worthwhile. It is crucial to bear this in mind, irrespective of whether anticoagulant therapy is being administered. A larger randomised trial must be conducted to prove the findings of this study.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the AME Case Series reporting checklist. Available at https://jeccm.amegroups.com/article/view/10.21037/jeccm-24-117/rc

Peer Review File: Available at https://jeccm.amegroups.com/article/view/10.21037/jeccm-24-117/prf

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://jeccm.amegroups.com/article/view/10.21037/jeccm-24-117/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. All procedures performed in this study followed the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patients or their relatives to publish this article. A copy of the written consent is available for review by the editorial office of this journal.

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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