Abstract
Introduction:
Acute pulmonary embolism (aPE) can lead to death if not quickly identified. The standard of care for evaluation of aPE includes a Computed Tomography Pulmonary Angiogram (CTPA). Ultrasonography has shown promise in obtaining the tricuspid annular plane systolic excursion (TAPSE) measurements which may be of clinical importance in patients with aPE. The objective of this study is to evaluate the diagnostic capability of TAPSE measurements for patients with suspicion for aPE
Methods:
We prospectively enrolled patients who presented to the Emergency Department with suspicion of aPE. Each patient underwent a point of care ultrasound (POCUS) where a TAPSE measurement was obtained, followed by CTPA. Based on the CTPA findings, patients were grouped into 3 categories: no aPE, clinically insignificant aPE, or clinically significant aPE.
Results:
We enrolled 87 patients in this study. Twenty-three (26.4%) of these patients were diagnosed with PE. Of patients with PE, fifteen (65%) were found to have a clinically significant aPE. Analysis of mean TAPSE measurements between patients with clinically significant aPE and those with insignificant or no PE was 15.2 mm and 22.7 mm, respectively (p=<0.0001). Following ROC curve analysis, optimum TAPSE measurement to identify clinically significant aPE is 18.2 mm. A cutoff TAPSE measurement of 15.2 mm shows a sensitivity of 53.33% (95% CI 26.67%−80.00%) and a specificity of 100% (95% CI 100%−100%) for the diagnosis of a clinically significant PE.
Conclusions:
Our data suggest that TAPSE measurements less than 15.2 mm have a high specificity for identifying clinically significant aPE.
Keywords: TAPSE, pulmonary embolism, right heart strain, cardiac ultrasound, Point of care ultrasound
INTRODUCTION
Acute pulmonary embolism (aPE) is an infrequent but potentially lethal diagnosis that is often made in the Emergency Department (ED). The mortality of patients diagnosed with aPE ranges from 5% for those who are clinically stable up to 58% for patients who are in critical condition [1–4]. Overall, aPE has a mortality of 1 in 1,000 individuals in the United States each year [5]. Diagnostic testing for these patients includes a combination of d-dimer, EKG and diagnostic imaging. Current standard of care for the diagnostic imaging confirmation of patients with suspected pulmonary embolism includes a Computer Tomography Pulmonary Angiogram (CTPA) scan or Ventilation-Perfusion (VQ) scan. CTPA however does not directly evaluate the right ventricle and, previous studies have explored the potential for point-of-care ultrasound (POCUS) to help identify evidence of right heart dysfunction as CTPA cannot directly evaluate right ventricular pressures or function [6].
In patients with clinically significant aPE, arterial occlusion may create a pressure overload that leads to increased right ventricle pressure causing right ventricular dilatation and decreased function of the right ventricle (RV) [7]. The burden of the clot occlusion can be manifested by decreased RV outflow, increased pulmonary vascular resistance, and increased RV wall stress [4]. This situation results in dilatation in the right ventricular outflow tract (RVOT) and increase in pulmonary artery pressure which can manifest as right ventricular dysfunction [8–10]. Patients with clinically insignificant PE may not exhibit any hemodynamic or structural cardiac changes however, patients with large clot burden may exhibit right ventricular dysfunction that can be identified with ultrasound.
For patients with suspicion of a pulmonary embolism, early diagnosis of aPE is useful to help guide management in the ED. While CTPA is currently the gold standard for making the diagnosis, there are several drawbacks including transport time to obtain the scan, exposure to ionizing radiation, inability to scan patients with renal insufficiency and the inability to scan hemodynamically unstable patients [11]. Given these limitations, ultrasound has been evaluated as an alternative, non-invasive modality to help evaluate right ventricular function.
The Tricuspid Annular Plane Systolic Excursion (TAPSE) has been studied as a surrogate measure for the assessment of right ventricular function. This technique consists of using M-mode echocardiography, which can be used to measure the movement of the tricuspid annulus of the right ventricle between the end of systole and end of diastole [4,12]. Previous studies done on healthy individuals without an aPE estimate the normal TAPSE value to be between 2.4cm and 2.6cm [13]. A lower TAPSE value represents decreased RV function [13]. TAPSE values have proven to have prognostic utility for patient outcomes and may be useful to identify patients with clinically significant RV dysfunction. Currently, several studies have evaluated the use of TAPSE for patients with aPE however, no previous studies have compared TAPSE values to clot burden.
The primary objective of this study is to evaluate the diagnostic capability of a TAPSE measurements for patients presenting to the ED with suspicion for aPE. A second objective of our study is to determine the correlation between the TAPSE value and mechanical clot burden.
MATERIAL AND METHODS
Study Design and Settings
We performed a prospective, observational single-site study utilizing a convenience sample of patients who presented to the ED between November 2015 and July 2017, in an urban university hospital ED, which supports an emergency medicine (EM) residency training program as well as an EM ultrasound fellowship. The annual ED census consists of approximately 57,000 patient visits with an ethnically and economically diverse patient population. The study was approved by the site institutional review board and presented following STARD guidelines.
Selection of Participants
Research associates reviewed the ED grease board for potential patients daily between the hours of 8:00 am and 12:00 midnight. Patients were eligible for inclusion if they were at least 18 years old, able to provide written and verbal consent in English or Spanish, and were undergoing CTPA for the evaluation of aPE. All laboratory tests and imaging studies were performed at the discretion of the ordering physician. Patients were excluded if they were pregnant, incarcerated or did not meet inclusion criteria. Patients were also excluded if they had a history of pulmonary hypertension, known pulmonary embolism or heart failure. The research associates obtained informed written consent from eligible patients after discussion of the study with the treating physician.
Study Protocol
Research associates approached the treating physician for patients with any of the common symptoms of aPE including chest pain, shortness of breath, syncope or palpitations. All eligible patients with clinical suspicion for aPE undergoing a CTPA were approached for enrollment in the study. Members of the research team approached patients and reviewed all exclusion criteria with patients prior to enrollment. Once verbal and written consent were obtained, research personal collected data using a systematic approach on a standard data abstraction sheet. Collected data included general demographics such as age, gender, BMI, as well as the measured echocardiographic measurements. The treating emergency physician (EP) then performed POCUS to measure the TAPSE value prior to obtaining any test results. All ultrasounds were performed by clinicians prior to the results of the CTPA.
We obtained TAPSE measurements using Mindray TE7 (Mindray North America, Mahwah, NJ) ultrasound machines with phased array transducer in the cardiac setting. All patients were placed in left lateral decubitus position in order to properly obtain an apical 4-chamber view of the heart. An M-mode sampling spike was placed at the right lateral border of the heart which generated simultaneous live B and M mode active tracings. We obtained the TAPSE by measuring the vertical height between the peak and trough in a single cardiac cycle (Figure 1).
Figure 1:
Image of M-mode ultrasound with measurement of TAPSE value.
A total of 33 unique practitioners to collected TAPSE measurements. This included EM attending physicians, resident physicians and ultrasound fellows. Prior to the enrollment of patients in the study, all EM physicians underwent a 30-minute didactic keynote (Apple) lecture followed by supervised hands-on scanning of three healthy volunteer adult models. All practitioners were required to demonstrate the ability to obtain an apical 4-chamber view and correctly take a TAPSE measurement on three models prior to enrolling patients.
After the subject consented for enrollment, TAPSE measurement value was immediately obtained by the treating physician. Following this, results of the patient’s CTPA were then recorded by the research associate. All point-of-care ultrasound images were archived and reviewed by the ED ultrasound director to confirm appropriate image quality and accurate measurements. The ED ultrasound director was blinded to CTPA results. The gold standard for the diagnosis of aPE in this study was the presence of a filling defect in the pulmonary arteries, as reported by the attending radiologist. Radiologists interpreting the CTPA were blinded to the results of the POCUS, and emergency physicians performing the POCUS were blinded to the results of the CTPA.
We grouped patients into three categories. The first group had no filling defects within the pulmonary arteries and were classified as negative for aPE. The second group had small, sub-segmental pulmonary embolisms of variable acuity without evidence of RV dysfunction on CTPA. These patients were classified as having a clinically insignificant aPE. The third group had clinically significant aPE which we defined as any of the following: aPE with large filling defects, PE located in the central location (segmental or proximal), saddle aPE, pulmonary infarction or CT evidence of RV dysfunction. CT evidence of RV dysfunction included interventricular septal bowing into the left ventricle, right ventricular enlargement or pulmonary trunk enlargement. These findings were defined by the final attending radiologist read of the CT scan.
Statistical Analysis
We summarized patient test characteristics as mean with standard deviation for continuous variables and frequency (percentage) for categorical variables in non-PE, clinically insignificant PE, clinically significant PE and overall. Furthermore, we used ANOVA (for continuous variables) and Chi-square test (for categorical variables) to compare the variables among three groups. We used the Two-sample t-test to compare TAPSE for PE vs. Non-PE and clinically significant vs. clinically insignificant + Non-PE. The overall difference of TAPSE among three groups was examined by ANOVA. We used Chi-square test to compare TAPSE among three categories (Non-PE, clinically insignificant and clinically significant). The study was powered to a total of at least 20 patients with aPE. This will provide 80% power to exclude a sensitivity 70% from a 95% confidence interval if the true sensitivity is 90%.
In order to show the predictive ability of TAPSE to distinguish between the three PE groups, we plotted an ROC curve for each two-group comparison and area under the curve with 95% confidence interval. The optimal cut-off was generated based on the point closest to the top-left part of ROC curve with weighted sensitivity and specificity. Weight was determined by relative cost (r = 4) and disease prevalence, where relative cost means relative loss of a false negative as compared with a false positive. Sensitivity and specificity were calculated from the ROC curve based on the optimal cut-off. We also presented 95% confidence interval of the sensitivity and specificity by 2000 bootstrap. Point estimate of sensitivity and specificity was calculated based on the data. We then used 2000 bootstrap to conduct the confidence interval. This included random resampling with replacement 2000 times and calculated the according ROC statistics for each resampling data.
RESULTS
We enrolled a total of 87 patients during the study period. All enrolled patients had CTPA performed as well as POCUS. Twenty-three (26.4%) of these patients were diagnosed with a pulmonary embolism. Of these patients, fifteen (65%) were found to have a clinically significant pulmonary embolism based on the aforementioned criteria. This included large, proximal embolus, as defined by the attending radiology report, evidence of right heart strain or pulmonary infarction. Both groups had similar baseline characteristics and initial heart rate and blood pressure readings were similar, although patients with a clinically significant pulmonary embolism had significantly lower initial pulse oximetry readings (Table 1).
Table 1.
Summary of patients’ characteristics among three groups and overall. Values listed are mean for each category with standard deviation.
| Non-PE (N = 64) |
Clinically insignificant PE (N = 8) |
Clinically significant PE (N = 15) |
Overall (N = 87) |
P-value | |
|---|---|---|---|---|---|
| Age (years) | 53 (16) | 50 (19) | 59 (18) | 54 (17) | 0.392 |
| Sex | |||||
| Female | 34 (53.1%) | 6 (75.0%) | 7 (46.7%) | 47 (54.0%) | 0.414 |
| Male | 30 (46.9%) | 2 (25.0%) | 8 (53.3%) | 40 (46.0%) | |
| Temperature (Celsius) | 36.7 (0.31) | 36.9 (0.24) | 36.8 (0.31) | 36.7 (0.30) | 0.361 |
| Heart Rate | 86 (21) | 84 (13) | 90 (20) | 87 (20) | 0.749 |
| Blood Pressure (mmHg) | |||||
| Systolic | 133 (19) | 129 (24) | 136 (21) | 134 (20) | 0.715 |
| Diastolic | 73 (14) | 76 (22) | 80 (15) | 75 (15) | 0.254 |
| Respiratory Rate | 20 (20) | 17 (2) | 18 (2) | 20 (17) | 0.807 |
| Pulse Ox | 97.7 (2.51) | 98.7 (1.16) | 96.1 (2.29) | 97.5 (2.47) | 0.027 |
| Weight (kg) | 82.3 (21.89) | 76.8 (18.38) | 95.3 (31.79) | 84.0 (23.93) | 0.109 |
| BMI | 29.3 (6.71) | 28.1 (6.05) | 33.5 (9.37) | 29.9 (7.29) | 0.104 |
Comparison of TAPSE measurements between patients with pulmonary embolism and no pulmonary embolism (Figure 2, boxplot) showed a mean TAPSE of 22.8 mm (SD 4.3 mm) for patients with no PE and 17.6 mm (SD 5.2 mm) for patients with PE which reached statistical significance (p=0.0002). Mean TAPSE measurements of patients with no PE, clinically insignificant PE and clinically significant PE (Figure 3, boxplot) was 22.8 mm (SD 4.3 mm), 22.2 mm (3.1 mm) and 15.2 mm (4.4 mm), respectively. There was no significant difference between the no PE and clinically insignificant PE groups (p=0.63), however a significant difference exists between all three groups (p<0.0001). An analysis of a combined group of patients with clinically insignificant or no pulmonary embolism (Figure 4, boxplot) shows a mean TAPSE of 22.7 mm (SD 4.2) as compared to a mean of 15.2 mm (SD 4.4) in patients with clinically significant PE (p=<0.0001).
Figure 2.
Boxplot of TAPSE between PE and Non-PE.
Figure 3.
Boxplot of TAPSE among non-PE, clinically insignificant PE and clinically significant PE.
Figure 4.
Boxplot of TAPSE between Non-PE, insignificant PE vs significant PE.
A receiver operating characteristic (ROC) curve analysis produced an optimal cutoff of 20.3 mm to identify all-comers with PE with a sensitivity of 71.88% (95% Confidence Interval [CI] 60.94%−82.81%) and specificity of 65.22% (95% CI 43.48%−82.61%) (Figure 5). Using ROC analysis, we further determined that an optimum TAPSE cutoff measurement to identify clinically significant PE is 18.2 mm which has a sensitivity of 83.33% (95% CI 73.61%−91.67%) and specificity of 80.00% (95% CI 60.00%−100.00%). A cutoff value of 15.2 mm shows a sensitivity of 53.33% (95% CI 26.67%−80.00%) and a specificity of 100% (95% CI 100%−100%) for the diagnosis of a clinically significant PE and a sensitivity of 34.78% (95% CI 17.39%−56.52%) and a specificity of 100% (95% CI 100%−100%) for diagnosis of any pulmonary embolism (Figure 6).
Figure 5.
ROC curve of TAPSE for PE vs. Non-PE
Figure 6.
ROC curve of TAPSE for significant PE, insignificant PE and non-PE.
DISCUSSION
Acute pulmonary embolism can be a potentially lethal diagnosis that is often made in the ED. Early recognition of this disease can lead to interventions such as thrombolysis, anticoagulation or clot retrieval. The current gold standard for the diagnosis of aPE remains CTPA [14]. However, in certain populations such as pregnant women, renal impairment, contrast allergies or hemodynamic instability, CTPA may not be suitable [15]. Increasingly, point of care ultrasound has been used to evaluate cardiac function and assess for aPE. However, direct visualization of the pulmonary arteries is not possible with POCUS. Thus, secondary signs associated with aPE such as RV dysfunction can be used to support the diagnosis when CTPA is contraindicated or not available. Previous studies have demonstrated that TAPSE can be used to objectively measure RV dysfunction [13, 16–18]. Park et al and Tamborini et al have found that a TAPSE value less than 17 mm to be indicative of RV dysfunction which can be indicative of sub-massive aPE [16,19]. The aim of this study was to determine if TAPSE values can be a diagnostic indicator of right heart strain for patient with suspicion for aPE in the Emergency Department.
In patients with clinically significant aPE, evaluation of the right ventricle for systolic dysfunction can yield significant information. Our data indicates that patients with clinically significant aPE had an average TAPSE value of 17.6 mm which is consistent with prior studies that correlated this value with RV systolic dysfunction. However, this historically accepted value is not specific for aPE and the best cut-off value for TAPSE has not been extensively examined. A recent study by Daley et al. (2017) concluded that the optimal cut-off value for TAPSE in PE is 20 mm with a sensitivity of 72% (95% CI 53–86) and a specificity of 66% (95% CI, 57–75) [20]. This data corresponds well with our cut-off value of 20.2 mm, with similar sensitivity and specificity. In our study, the optimal cut-off value for identifying clinically significant aPE was 18.2 mm, which yielded a sensitivity of 83.33% and specificity of 80.00% as compared to the optimal cut-off value for all comers with PE.
Given that 26.4% of all patients who underwent CPTA for evaluation of aPE were found to be positive for aPE, our data indicates that using TAPSE in conjunction with clinical evaluation and risk stratification tools such as the Well’s criteria and the modified Geneva score may increase the pretest probability for diagnosis of PE. A TAPSE value below the observed threshold of 18.2 mm may increase the pretest probability for aPE. Our data shows that the mean TAPSE measurements of patient with no aPE or clinically insignificant PE was essentially the same with no statistical significance. Thus, if the presence of clinically insignificant PE is of interest to the clinician, additional imaging should be considered as TAPSE should not be used to differentiate between clinically insignificant PE and lack of PE. For patients with clinically significant aPE, the TAPSE value may be severely diminished. Previous studies have already shown that the higher embolic burden of PE is associated with higher mortality and increased right ventricular dysfunction [21–23]. Thus, a finding of decreased TAPSE value in patients with high clinical suspicion for aPE may be useful to initiate early anticoagulant therapy before CTPA, and also may help obviate a closer level of monitoring such as the intensive care unit.
Based on our data, TAPSE values may be of prognostic value to stratify patients into categories based on RV dysfunction. Patients with significantly diminished TAPSE values may be at high risk for deterioration and can be candidates for fibrinolysis or clot retrieval. Conversely, patients with clinically insignificant PE and normal TAPSE values may be considered low risk and some may even be candidates for outpatient anticoagulation. Future large-scale trials are needed to continue to evaluate the role of TAPSE in the evaluation and management of aPE. Additional studies may be useful to further validate the reliability of TAPSE measurements and compare TAPSE to cardiology-performed 2D echo for the evaluation of right ventricular dysfunction [24].
LIMITATIONS
This study was limited by recruitment of subjects from a convenience sample of patients at a single center, which may introduce selection bias and decrease the external validity and generalizability. Our study did not seek to determine the amount of training required for proficiency in obtaining or interpreting TAPSE values. Measurements can be affected by operator experience and we did not assess for inter-rater reliability in this study. Additional findings or studies such as cardiology performed echo that can suggest right heart strain such as RV dilatation, EKG and troponin were not recorded or evaluated for study purposes. CT scan can only capture one point in time and is not the criterion standard to assess for right ventricular dilatation. We were unable to study patients who did not undergo CPTA including pregnant women, patients with renal insufficiency, contrast allergies or prisoners, thus our results may not be applied to these populations.
CONCLUSION
In patients presenting to the ED with clinical suspicion for aPE, the optimum TAPSE value to assess for clinically significant aPE is 18.2 mm. Using a cut off of 15.2 mm TAPSE has a sensitivity of 53.33% and a specificity of 100% for the diagnosis of a clinically significant PE. For patients with clinically insignificant PE, TAPSE may not be useful due to the lack of RV dysfunction.
ACKNOWLEDGEMENTS
The authors would like to thank the Emergency Medicine Research Associates Program (EMRAP) for assisting with data collection and assisting with patient enrollment. Data analysis was also supported by the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant UL1 TR000153. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.
Financial Support: No authors received any financial support as part of this project. Data analysis was supported by the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant UL1 TR000153.
Acknowledgments: UC Irvine Health Department of Emergency Medicine, UC Irvine School of Medicine
Footnotes
Disclosures: Dr. J Christian Fox receives stock options from Sonosim for consulting. However, no Sonosim products were used in this research project. No other authors have any financial disclosures.
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