Clinical and echocardiographic predictors of mortality in acute pulmonary embolism
Dahhan et al. Cardiovascular Ultrasound
Clinical and echocardiographic predictors of mortality in acute pulmonary embolism
Talal Dahhan 0 4
Irfan Siddiqui 3
Victor F. Tapson 2
Eric J. Velazquez 1
Stephanie Sun 5
Clemontina A. Davenport 5
Zainab Samad 1
Sudarshan Rajagopal 0 1
0 Center for Pulmonary Vascular Disease , Box 102351, DUMC, Durham, NC 27710 , USA
1 Department of Medicine, Division of Cardiology, Duke University , Durham, NC , USA
2 Department of Medicine, Division of Pulmonary and Critical Care Medicine, Cedars Sinai Medical Center , Los Angeles, CA , USA
3 Department of Medicine, East Carolina University , Greenville, NC , USA
4 Department of Medicine, Division of Pulmonary, Allergy and Critical Care Medicine, Duke University , Durham, NC , USA
5 Department of Biostatistics and Bioinformatics, Duke University Medical Center , Durham, NC , USA
Purpose: The aim of this study was to evaluate the utility of adding quantitative assessments of cardiac function from echocardiography to clinical factors in predicting the outcome of patients with acute pulmonary embolism (PE). Methods: Patients with a diagnosis of acute PE, based on a positive ventilation perfusion scan or computed tomography (CT) chest angiogram, were identified using the Duke University Hospital Database. Of these, 69 had echocardiograms within 24-48 h of the diagnosis that were suitable for offline analysis. Clinical features that were analyzed included age, gender, body mass index, vital signs and comorbidities. Echocardiographic parameters that were analyzed included left ventricular (LV) ejection fraction (EF), regional, free wall and global RV speckle-tracking strain, RV fraction area change (RVFAC), Tricuspid Annular Plane Systolic Excursion (TAPSE), pulmonary artery acceleration time (PAAT) and RV myocardial performance (Tei) index. Univariable and multivariable regression statistical analysis models were used. Results: Out of 69 patients with acute PE, the median age was 55 and 48 % were female. The median body mass index (BMI) was 27 kg/m2. Twenty-nine percent of the cohort had a history of cancer, with a significant increase in cancer prevalence in non-survivors (57 % vs 29 %, p = 0.02). Clinical parameters including heart rate, respiratory rate, troponin T level, active malignancy, hypertension and COPD were higher among non-survivors when compared to survivors (p ≤ 0.05). Using univariable analysis, NYHA class III symptoms, hypoxemia on presentation, tachycardia, tachypnea, elevation in Troponin T, absence of hypertension, active malignancy and chronic obstructive pulmonary disease (COPD) were increased in non-survivors compared to survivors (p ≤ 0.05). In multivariable models, RV Tei Index, global and free (lateral) wall RVLS were found to be negatively associated with survival probability after adjusting for age, gender and systolic blood pressure (p ≤ 0.05). Conclusion: The addition of echocardiographic assessment of RV function to clinical parameters improved the prediction of outcomes for patients with acute PE. Larger studies are needed to validate these findings.
Echocardiography; Pulmonary embolism; Right ventricular function; Speckle-tracking echocardiography
Acute pulmonary Embolism (PE) is a major cause of
morbidity and mortality in the United States and
Europe, accounting for 100,000 and 300,000 deaths
annually, respectively [1, 2]. PE can be classified as massive,
submassive or nonmassive based on the hemodynamic
status and right ventricular (RV) function of the patient.
Massive PE is characterized by systemic hypotension or
cardiogenic shock, submassive PE is characterized by RV
dysfunction without hypotension, and nonmassive PE
has neither systemic hypotension nor RV dysfunction
. Massive PE is associated with an in-hospital
mortality of 25–50 %, submassive PE with a mortality rate of
3–15 %, while nonmassive PE is associated with
mortality of 5 % or less . Risk assessment in patients with
submassive PE can be difficult, as the mortality rates for
submassive PE can approach that of massive PE .
While there is a consensus that systemic thrombolysis,
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catheter-directed interventions, or surgery are indicated
in patients with massive PE, the management of patients
with submassive PE remains controversial. Therefore,
there remains a challenge in the clinical management of
patients who have stable hemodynamics but
demonstrate evidence of RV dysfunction, either by
electrocardiogram, echocardiogram, computed tomography (CT)
scan or cardiac biomarkers . The benefit of
thrombolytic or invasive therapies relative to the risk of bleeding
is unclear among such patients . An improved
approach to risk assessment could therefore allow the
identification of those patients presenting with
submassive PE who would benefit most from therapy.
To address this, risk assessments based on clinical and
imaging parameters have been developed. The Pulmonary
Embolism Severity Index (PESI) is an excellent clinical
predictor of outcomes in patients with PE . It is based
on 11 clinical criteria including age, sex, history of cancer
and hemodynamic parameters. Five risk categories are
included, ranging from very low risk, with 30-day mortality
of less than 2 %, to very high risk, with 10.0–24.5 %
mortality . The simplified PESI (sPESI) was subsequently
developed, with only six, rather than 11, clinical criteria.
In this index, only two risk categories were included, with
low risk associated with 1.1 % mortality and high risk
associated with an 8.9 % risk of death . Quantitative
echocardiographic assessment has been gaining
importance in patients with RV dysfunction, including those with
congenital heart disease, pulmonary hypertension and
pulmonary embolism [8, 9]. A number of studies [10–21]
have tested the utility of novel echocardiographic or
serum biomarkers for risk assessment in acute PE, but
only a few studies have tested whether such parameters
provide additional benefit to clinical predictors [22, 23].
We hypothesized that the addition of quantitative
echocardiographic markers of RV function would add to
clinical parameters to predict outcomes in patients with
We retrospectively identified patients who had a
diagnosis of acute PE between January 2010 and April 2014,
confirmed by contrasted computed tomography (CT)
scan of the chest and/or ventilation-perfusion (VQ)
nuclear medicine imaging at Duke University Medical
Center (Durham, NC, USA) using the Duke Enterprise
Data Unified Content Explorer (DEDUCE) . Subjects
were included in the study if they had an
echocardiogram performed within 24–48 h of diagnosis of acute
PE. Subjects were excluded if their echocardiographic
images were suboptimal for RV strain measurement due
to poor image quality or poor RV views. Clinical data
including demographics, medical history, comorbidities,
systemic blood pressure, heart rate, respiratory rate,
oxygen saturation on room air and with supplemental
oxygen, were collected from the medical record. The
Duke University Medical Center Institutional Review
Board approved this study.
Echo-derived parameters of RV function
All echocardiographic studies were performed on GE
Vivid E9 using a 3.5 MHz probe (GE, Vingmed
Ultrasound, Hortom, Norway) or Philips IE33 (Philips,
Netherlands). Off-line analyses of images were
performed in Xcelera (Philips, Andover, MA) and
ImageArena (TomTec Imaging Systems, Unterschleißheim,
Germany) by a single experienced reader and analysis
was confirmed by a separate experienced reader;
interreader variability for these studies have been shown to
be low . TAPSE was determined from an M-mode
through the lateral tricuspid annulus by calculating the
amount of longitudinal motion of the annulus at peak
systole  (Fig. 1a). RV Tei index was calculated as the
RV isovolumic time (IVT) divided by the ejection time
(ET) using the pulsed Doppler method  (Fig. 1c). IVT
was calculated as the duration of tricuspid regurgitation
from continuous wave Doppler across the tricuspid valve
minus the ET from a single representative beat. ET was
calculated as the duration of RV outflow on pulsed
Doppler across the RVOT from a single representative
beat (Fig. 1c). Care was taken to use beats with similar
RR intervals to minimize errors in calculation. RV
Fraction Area Change (FAC)  was calculated as the
[(RV end-diastolic area – end-systolic area)/end-diastolic
area] × 100 (Fig. 1d). The RV endocardium was traced
in systole and diastole from the annulus, along the free
wall, to the apex and back along the interventricular
septum using the apical four-chamber view. Attempts
were made to trace the free wall beneath trabeculations
RV longitudinal strain
2D strain analysis was performed from the apical
4chamber view as previously described  (Fig. 1b). The
reference point for a single cardiac cycle was placed at
the beginning of the QRS. Pulmonic valve closure was
determined from the pulsed wave Doppler profile of the
RV outflow tract. The endocardial border was traced in
end systole and the region of interest was adjusted to
exclude the pericardium. The quality of the tracking was
confirmed visually from 2D images and from the strain
traces. Segments with persistently inadequate tracking
despite attempts at improving border definition and
region of interest were excluded from analysis. The
longitudinal strain of the RV free wall (RVfree) was calculated
as the average of the three free wall segments and the
longitudinal strain of the RV septum (RVsept) was
Fig. 1 Different 2D echocardiographic methods used in this study to assess RV function. a Tricuspid Annular Plane Systolic Excursion (TAPSE) is
determined from an M-mode image through the lateral tricuspid annulus by calculating the amount of longitudinal motion of the tricuspid
annulus at peak systole. b RV longitudinal strain is calculated from speckle-tracking of an RV focused apical 4-chamber view. c RV Tei index is
calculated as the RV isovolumic time (equal to tricuspid regurgitation duration (TRd) – ejection time (ET)) divided by the ET using the pulsed
Doppler method. d RV Fractional Area Change (RV FAC) was calculated as the [(RV end-diastolic area – end-systolic area)/end-diastolic area] × 100
calculated as the average of the three septal segments.
Global RVLS was calculated as the average of strains
from all segments. All strain and other 2D echo-derived
parameter analyses were performed blinded to clinical
Demographic and clinical characteristics of participants
were presented in the study by survival status and the
two groups were compared using Fisher’s exact test for
categorical variables and a Kruskal-Wallis rank sum test
for continuous variables. Continuous variables were
summarized by the median and interquartile range and
categorical variables were summarized by counts and
percentages (Tables 1 and 2). Table 3 displays the odds
ratios and 95 % confidence intervals resulting from
univariable logistic regression modeling the probability of
survival. These models investigated the association
between clinical characteristics, cardiac biomarkers,
specific echocardiographic features and PESI predictor
score on the probability of survival and no adjustment
for multiple testing was done. Multivariable models were
fit to investigate the effects of some clinical features with
echocardiographic parameters on survival, and the
results are shown in Table 4. Statistical analyses were
performed using SAS 9.4 (SAS, Cary, NC) and R (R Core
Team (2015), Vienna, Austria).
During the study period, 135 patients were admitted with a
clinical diagnosis of acute PE. Among these, 95 patients
diagnosed with an acute PE had a transthoracic
echocardiogram within the initial 24–48 h of admission. 26 patients
did not have suitable images for offline analysis, resulting
in a cohort of 69 analyzed subjects. Six of the subjects
underwent thrombolysis. At 30 days, of these 69 subjects,
14 had died and 55 survived. (Table 1).
Baseline characteristics and presentation
The baseline characteristics of all 69 patients are listed in
Table 1. The median age was 55 years old (range 16–95)
and 48 % (n = 38) of patients were females. The median
body mass index (BMI) was 27 kg/m2 (range 20–68). With
respect to comorbidities, 29 % (n = 20) of the cohort had a
history of cancer, with a significantly higher prevalence
in non-survivors compared to survivors (57 % vs. 29 %,
p = 0.02). The only other significant difference in
comorbidities between non-survivors and survivors was
in the prevalence of hypertension (non-survivors, 64 %,
vs. survivors, 25 %, p = 0.03). 13 % of patients (n = 9)
had a history of prior venous thromboembolism. On
presentation, 90 % (n = 62) had NYHA class III
symptoms (Table 1). Hypoxemia on presentation,
tachycardia, tachypnea, elevation in Troponin T, absence of
hypertension, active malignancy and chronic
Table 1 Baseline characteristics for the cohort of patients with acute PE
Age at Diagnosis (69)
Body Mass Index (69)
Systolic Blood Pressure (66)
Diastolic Blood Pressure (66)
Fraction of Inspired Oxygen (69)
Troponin T level (ng/mL) (23)
Essential Hypertension (69)
Type II Diabetes (69)
Chronic Kidney Disease (69)
Previous Venous Thromboembolism (69)
Connective Tissue Disease (69)
Active Malignancy (69)
Orthopedic Fracture or Injury (69)
Chronic Obstructive Pulmonary Disease (69)
Pulmonary Embolism Severity Index (PESI) class (69)
Shown are median and inter-quartile range in brackets or number of patients with percent of patients in parentheses. P-value denotes comparison between
nonsurvivors and survivors
Abbreviations: NYHA New York Heart Association
obstructive pulmonary disease (COPD) were
statistically significantly different (p ≤ 0.05) between
nonsurvivors and survivors (Table 1).
Echocardiographic assessment of RV function in acute PE
A number of echocardiographic parameters were
assessed in our cohort (Table 2). These included
parameters that are thought to quantify RV systolic
function (TAPSE, global, regional and free wall RV
longitudinal strain (RVLS), RV myocardial
performance (Tei) Index, RV fraction area change (RVFAC),
and subjective echocardiographic evaluation of RV
function) and RV size (RV/LV ratio in systole and
diastole, diameters of RV and LV in systole and diastole).
RVFAC, Tei Index, global and free wall RVLS were
significantly different between survivors and
nonsurvivors (p ≤ 0.05). For example, a significant proportion
of non-survivors had global and free wall RVLS of
more than −12.5 (Fig. 2), a value which has been
demonstrated to be associated with worse outcomes
in pulmonary hypertension . TAPSE, subjective
RV dilation and subjective RV dysfunction were not
statistically different between survivors and
nonsurvivors (p > 0.05).
Univariable and multivariable predictors of outcome in
On univariable analysis, a number of clinical and
echocardiographic parameters were statistically significantly
(p ≤ 0.05) associated with 30 day mortality. These
included active malignancy, serum troponin, global and
free wall RVLS, RV Tei Index, and patients with PESI
classes four and five. For multivariable regression
analysis, we attempted to include PESI as a clinical
predictor with selected echo parameters, but could not
because PESI score (whether categorical or continuous)
demonstrated non-trivial collinearity with global and
free wall RVLS and RV Tei index, resulting in unstable
standard errors of estimates. Similarly, both heart rate
and systolic blood pressure displayed significant
collinearity, so only systolic blood pressure was included as it
was a predictor in the univariable model. As the
multivariable models could not include those clinical
and echocardiographic predictors together, we instead
used a multivariable model that included parameters
used to calculate PESI , namely age, gender and
systolic blood pressure. With this multivariable regression
model, global and free wall RVLS and RV Tei index all
predicted outcome with statistical significance (p ≤ 0.05).
This study demonstrates that the addition of selected
echocardiographic estimates of RV function to clinical
parameters in patients with acute PE improved
prediction of 30-day mortality in a cohort of patients with
acute PE. In our cohort, global, free wall RVLS and RV
Tei index analyses were independently associated with
mortality on univariable and multivariable analysis.
However, other assessments of RV function, including
Systolic Blood Pressure
Free wall RVLS model
Systolic Blood Pressure
RV Tei Index model
Systolic Blood Pressure
Table 4 Multivariable analysis of clinical and echocardiographic parameters in predicting outcome in acute PE
Odds ratio (survival over non-survival), 95 % confidence interval, estimate, standard error, and p-value of the multivariable logistic regression models are shown
TAPSE, RVFAC, and subjective evaluations of RV size
and function were not associated with mortality on
univariable analysis. At this time, there are no clear
guidelines as to which parameters should be used to assess
RV function , and significant inter-rater variability
exists in subjective evaluation of the RV . The objective
echocardiographic assessment of RV function with
Fig. 2 a Global Right Ventricular Strain (RVLS) and b free wall RVLS
categorized as mild, moderate and severe among survivors and
nonsurvivors in a cohort of patients with acute pulmonary embolism
qualitative parameters, such as RVLS, may reduce
interrater variability  and have utility in identifying
submassive PE patients who may benefit most from
consideration of aggressive therapies.
The European Society of Cardiology  and the
American College of Chest Physicians guidelines  emphasize
the importance of the assessment of RV function and
cardiac biomarkers in risk assessment of acute PE, as they
may allow the identification of high-risk patients before
they clinically deteriorate. An alternative strategy has been
the use of clinical risk prediction algorithms, such as PESI
and sPESI [6, 7]. In our analysis, we found significant
collinearity between PESI and RVLS and Tei index,
suggesting that these echocardiographic and clinical
parameters are all associated with high risk features.
While global and free wall RVLS require special software
and analysis to obtain, RV Tei index is relatively
straightforward to acquire and could be used broadly. Vitarelli et
al. found an association of a number of parameters of RV
function with 6 month adverse outcomes in acute PE
patients on univariate analysis . Moreover, they found
that mid-free wall RVLS, RVSP and 3D RV ejection
fraction were associated with adverse outcome on multivariate
analysis. While we observed large absolute numerical
differences in basal free wall strain between survivors and
nonsurvivors, they did not reach statistical significance
due to large variance. It is likely that they would have been
significant in a larger study. Overall, the results here
extend the findings of Vitarelli et al., as we found that both
global and free wall RVLS were associated with outcome
on multivariable analysis after accounting for age, gender
and systolic blood pressure.
While subjective RV dysfunction has been associated
with worse outcomes in PE , a number of studies
suggest that quantifiers of RV function may better
identify high-risk patients, although most of these studies
did not test the utility of such parameters in
combination with clinical characteristics [11, 13–21]. For
example, RV dysfunction, as assessed by tricuspid annular
plane systolic excursion (TAPSE) and RV myocardial
performance (Tei) index, has been characterized in
patients with PE [32, 33]. Another recent study
identified the ratio of RV to LV end-diastolic diameter, RV
systolic pressure, tricuspid annular plane systolic excursion,
and inferior vena cava collapsibility to be independently
associated with mortality in patients presenting with
acute PE . Abnormal RV global and free wall
speckle-tracking strains have been associated with
adverse events in patients with PE . Ozsu and
coworkers demonstrated a correlation of Tei index with
treatment response in acute PE . Park and coworkers
demonstrated that TAPSE correlated with other
parameters of RV function and BNP in acute PE . RV
ejection fraction and regional mid wall strain has been
prospectively assessed in patients with PE, with a
potential to assess a therapeutic response . Thus, there are
a number of parameters of RV function that have been
shown to correlate with outcomes in acute PE.
Although our cohort of patients is small, we found an
association of free-wall, global RV strain and RV Tei
index with mortality. Notably, we did not find such a
relationship between other measures, including TAPSE,
RV size and RV/LV ratio. The associations we found
were still significant after the inclusion of clinical risk
factors [6, 7]. These findings suggest that the addition of
echocardiographic parameters to clinical parameters
may improve risk prediction in acute PE.
Our study is a retrospective, single center study with a
small cohort of patients, which may limit the
generalizability of these findings. Patient care was
variable, resulting in significant differences in studies that
were performed, such as troponin T, which was only
performed in 23 of the 69 subjects included in the final
analysis. As there was no set protocol for RV imaging in
this retrospective study, there was a relatively low
suitability (72.6 %) of images for offline analysis and poor
tracking observed in the basal and mid-free wall
segments. In our analysis, we found significant collinearity
between PESI and RVLS and Tei index, preventing us
from combining our echo predictors with PESI score.
Therefore, it is possible that echo predictors do not add
significant information to the PESI score. Previous
studies from our group have demonstrated small
interand intra-observer variability in assessment of RV strain
, so such analyses were not included in this study.
Future prospective, multi-center studies that address
objective RV function assessment in relation to outcomes
in patients with PE are needed to validate these findings.
2D: Two dimensional; 3D: Three dimensional; BNP: Brain natriuretic peptide;
COPD: Chronic obstructive pulmonary disease; CT: Computed tomography;
DEDUCE: Duke Enterprise Data Unified Content Explorer; EF: Ejection fraction;
ET: Ejection time; GE: General electric; IVT: Iso volumic time; LV: Left ventricle;
PAAT: Pulmonary artery acceleration time; PE: Pulmonary embolism;
PESI: Pulmonary embolism severity index; RV: Right ventricle; RVFAC: Right
ventricular fraction area change; RVLS: Right ventricular longitudinal strain;
RVOT: Right ventricular outflow tract; SAS: Statistical analysis system software;
sPESI: simplified pulmonary embolism severity index; TAPSE: Tricuspid
annular plane systolic excursion; VQ: Ventilation perfusion
Ethics approval and consent to participate
This study was approved by the institutional review board at Duke
University. All the data are available as stored within a secure drive that is
shared the among study authors.
Funding was obtained from NIH grants K08HL114643, Gilead Research
Scholars in Pulmonary Arterial Hypertension and a Burroughs Welcome
Career Award for Medical Scientists supporting Sudarshan Rajagopal, the
corresponding author. Clemontina Davenport is partially supported by Duke
CTSA grant UL1TR001117.
TD, ZS and SR designed the study. TD collected data and wrote the
manuscript. IS collected data, performed the echocardiographic analysis. SS
and CD performed the statistical analysis. VT, EV, ZS and SR reviewed and
edited the manuscript. All authors read and approved the final manuscript.
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