European Heart Journal - Cardiovascular Imaging (2020) 00, 1–10

doi:10.1093/ehjci/jeaa243

The echocardiographic ratio tricuspid annular

plane systolic excursion/pulmonary arterial

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systolic pressure predicts short-term adverse
outcomes in acute pulmonary embolism
Mads D. Lyhne 1,2,3*, Christopher Kabrhel1, Nicholas Giordano1, Asger Andersen2,
Jens Erik Nielsen-Kudsk2, Hui Zheng4, and David M. Dudzinski1,3*
1
Department of Emergency Medicine, Center for Vascular Emergencies, Massachusetts General Hospital, 0 Emerson Place, MA 02114, USA; 2Department of Cardiology, Aarhus
University Hospital, Palle Juul Jensens Boulevard 99, 8200, Aarhus N, Denmark; 3Department of Cardiology, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114,
USA; and 4Biostatistics Center, Massachusetts General Hospital, 50 Staniford Street, Boston, MA 02114, USA

Received 29 March 2020; editorial decision 3 August 2020; accepted 7 August 2020

Aims Right ventricular (RV) failure causes death from acute pulmonary embolism (PE), due to a mismatch between RV
systolic function and increased RV afterload. We hypothesized that an echocardiographic ratio of this mismatch
[RV systolic function by tricuspid annular plane systolic excursion (TAPSE) divided by pulmonary arterial systolic
pressure (PASP)] would predict adverse outcomes better than each measurement individually, and would be useful
for risk stratification in intermediate-risk PE.
...................................................................................................................................................................................................
Methods This was a retrospective analysis of a single academic centre Pulmonary Embolism Response Team registry from
and results 2012 to 2019. All patients with confirmed PE and a formal transthoracic echocardiogram performed within 2 days
were included. All echocardiograms were analysed by an observer blinded to the outcome. The primary endpoint
was a 7-day composite outcome of death or haemodynamic deterioration. Secondary outcomes were 7- and 30-
day all-cause mortality. A total of 627 patients were included; 135 met the primary composite outcome. In univari-
ate analysis, the TAPSE/PASP was associated with our primary outcome [odds ratio = 0.028, 95% confidence inter-
val (CI) 0.010–0.087; P < 0.0001], which was significantly better than either TAPSE or PASP alone (P = 0.017 and
P < 0.0001, respectively). A TAPSE/PASP cut-off value of 0.4 was identified as the optimal value for predicting ad-
verse outcome in PE. TAPSE/PASP predicted both 7- and 30-day all-cause mortality, while TAPSE and PASP did
not.
...................................................................................................................................................................................................
Conclusion A combined echocardiographic ratio of RV function to afterload is superior in prediction of adverse outcome in
acute intermediate-risk PE. This ratio may improve risk stratification and identification of the patients that will suf-
fer short-term deterioration after intermediate-risk PE.
..
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*Corresponding authors. Tel: þ1 (617) 643 0853. E-mail: ddudzinski@mgh.harvard.edu (D.M.D.); Tel: þ45 (204) 50486. E-mail: mads.dam@clin.au.dk (M.D.L.)
C The Author(s) 2020. For permissions, please email: journals.permissions@oup.com.
Published on behalf of the European Society of Cardiology. All rights reserved. V
2 M.D. Lyhne et al.

Graphical Abstract

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...........................................................................................................................................................................................
Keywords acute pulmonary embolism • right ventricular function • echocardiography • risk stratification • right
ventricular afterload

.. limited to a range of 40–80%9,13,14 and additional prognostic

Introduction ..
.. measures are needed.
Pulmonary embolism (PE) is the third leading cause of cardiovascular
.. For accurate prognosis in PE, it is likely important to investigate the
..
mortality. Death following acute PE is due to right ventricular (RV) .. RV and pulmonary circuit as one combined physical unit.15 Failure to
..
dysfunction and failure.1,2 Abrupt increases in RV afterload from the .. do so may be a reason that existing approaches fall short. Accordingly,
combined consequences of pulmonary arterial (PA) mechanical ob- .. in this investigation, we sought to define a marker that simultaneously
..
struction and vasoconstriction3–5 may exceed the ability of the ven- .. characterizes changes in RV function and in RV afterload, by deriving
tricle to compensate.2,4,6 .. the echocardiographic index TAPSE/PASP. This ratio has been investi-
..
Minimally invasive tools, including biomarkers, electrocardiog- .. gated in conditions of left ventricular (LV) failure16–22 and in a few stud-
raphy, computed tomography, and especially transthoracic echo- ..
.. ies of chronic pulmonary arterial hypertension (PAH).23,24 We
cardiography (TTE)2,7–9 are used to predict adverse outcomes in .. hypothesized that TAPSE/PASP can predict adverse clinical outcomes
patients with acute PE. Using TTE, general RV function is inferred
..
.. in patients with acute PE better than TAPSE or PASP individually.
by tricuspid annular plane systolic excursion (TAPSE), RV dilata- ..
..
tion, inter-ventricular septal geometry, and pulmonary arterial sys- ..
tolic pressure (PASP).10 Such methods are intended to define ..
.. Methods
low-risk patient subgroups and to identify those initially normo- ..
tensive patients at high-risk of deterioration who merit advanced .. Design
..
therapeutic options.11,12 However, the sensitivity and specificity of .. This study is based on prospectively enrolled patients with PE from the
existing tools for predicting these adverse PE-related outcomes is
.. Pulmonary Embolism Response Team (PERT) registry at Massachusetts
The echocardiographic ratio TAPSE/PASP in acute pulmonary embolism 3

General Hospital (MGH), Boston.25 The registry was approved by the

.. echocardiographic measurements and outcome was investigated by logis-
..
Institutional Review Board of Partners HealthCare Inc. (no. .. tic regression models. We produced receiver operator curves (ROC)
2016P000179). .. and used the area under the curve (AUC) to test if the ratio TAPSE/PASP
..
Adult patients were included if they had both PE confirmed and a for- .. better predicted outcome than each parameter separately. Optimal cut-
mal TTE performed within 2 days of PERT activation. Patients were .. off point on the ROC was determined as the point that maximizes overall
enrolled from registry inception October 2012 through 31 January 2019.
.. sensitivity þ specificity; its 95% confidence interval calculated by a boot-
..
Patients were excluded if thrombus-reducing intervention (e.g. thromb- .. strap method with 2000 samples. Multivariate logistic regression analysis
olysis) or extracorporeal membrane oxygenation (ECMO) was done .. was performed adjusting for age, sex, smoking status, and past-medical
..
prior to TTE; or if image quality was deemed too poor for analysis. .. history of chronic obstructive pulmonary disease, asthma, and pulmonary

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.. hypertension. We calculated intra-class-correlation (ICC) for intra-
..
Outcomes .. observer variation analysis. SAS 9.4 (SAS Institute, Inc., Cary, NC, USA)
The primary endpoint was a 7-day composite outcome of all-cause mor- .. was used. A P-value <0.05 was considered statistically significant.
tality and PE-related clinical deterioration, defined as systemic systolic
..
..
hypotension <90 mmHg, need for inotropes or vasopressor, intubation ..
with mechanical ventilation, or need for rescue therapy including systemic .. Results
..
thrombolysis, catheter-directed therapy (CDT), surgical pulmonary em- ..
bolectomy (SPE), or ECMO; all to occur after PERT activation. .. Of 1072 PERT activations, 627 patients were included in analysis
..
Secondary outcomes were 7- and 30-day all-cause mortality. .. (Figure 1). Of these, 135 (22%) patients met the primary endpoint
.. within 7 days, including 25 (4%) deaths, 12 (2%) systemic thromboly-
..
Echocardiography .. sis, 62 (10%) CDT, 18 (3%) SPE, 8 (1%) ECMO, 34 (5%) new initiation
As a registry study, TTE ordering was not governed by protocol, but ra- .. of mechanical ventilation, and 14 (2%) requiring vasopressor due to
ther requested by the treating clinician or on the recommendation of the
..
.. systemic hypotension; a patient could have had more than one end-
PERT team at the time of PERT activation. .. point. At 30 days, 58 (9%) patients died.
Retrospective analyses of TTEs were performed on an offline worksta-
..
..
R
tion (SyngoV Dynamics, version VA20F, Siemens Healthcare GmbH, .. Demographics
Germany) blinded to clinical outcome. Analyses compiled with consensus ..
.. Demographics of the patients are shown in Table 1. Patients who met
echocardiographic interpretation recommendations,10,26 and values rep- ..
resented average of at least three cardiac cycles, or more in the case of .. and did not meet the primary outcome were generally comparable in
an irregular rhythm. TAPSE was measured on M-mode images as the dif-
.. terms of past medical history and risk factors.
..
ference in RV basal motion from peak systole to end-diastole. If no M- .. Table 2 shows the clinical presentation of patients at time of PERT
mode was recorded, TAPSE was measured manually on apical four- .. activation. Patients with adverse outcome had more frequently hyp-
..
chamber view images. RV and LV diameters were measured in end- .. oxia, tachycardia, tachypnoea, and elevated biomarkers.
diastole at the level of tip of the atrioventricular valve leaflets to generate ..
RV/LV ratio. The maximal tricuspid regurgitation velocity (TRV) by
..
.. Echocardiographic results
continuous-wave Doppler was used to derive the right atrial (RA)–RV .. Echocardiographic measurements are shown in Table 3. ICC values
pressure gradient by simplified Bernoulli equation. Inferior vena cava ..
(IVC) diameter was measured at the level of the hepatic veins. RA pres- ... were 0.97 for PASP, 0.98 for TRV, 0.95 for TAPSE, and 0.96 for
..
sure (RAP) was estimated as recommended.26 RAP was assumed to be ..
3 mmHg if the IVC was not recorded (n = 88) in order not to bias in fa- ..
vour of the TAPSE/PASP ratio. PASP was then calculated as the sum of
..
..
RAP and RA–RV pressure gradients, as no patient had pulmonic valve ..
stenosis. The ratio TAPSE/PASP was derived for each subject. ..
..
Fifty randomly selected TTE recordings were analysed serially in ..
blinded fashion to characterize intra-observer variability. ..
..
..
Other clinical parameters ..
..
History, examination findings, and laboratory values were obtained as per ..
routine clinical care. Only blood samples taken on the day of PERT activa- ..
tion were included. Due to an institutional change in troponin assay dur-
..
..
ing the timeframe of the study, troponin was considered elevated if ..
>_14 pg/mL (new assay) or >_0.03 ng/mL (prior assay). NT-proBNP was ..
..
considered elevated if >_600 pg/mL.2 A patient was considered biomarker ..
positive if either troponin or NT-proBNP was elevated. ..
..
..
Statistics ..
Data were analysed for normality by Shapiro–Wilk test. As most of the
..
..
vital sign and echocardiographic parameters were non-normally distrib- ..
uted, median (interquartile ranges) are presented. Patient groups with .. Figure 1 Flowchart of included patients. Flow of patients
.. included in the study. PE, pulmonary embolism; TTE, transthoracic
and without the primary outcome were compared by t-test or Mann– .. echocardiogram; TOE, transoesophageal echocardiogram.
Whitney U test for numerical covariates and v2 test or Fisher’s exact test ..
for categorical covariates, where appropriate. Correlation between
..
4 M.D. Lyhne et al.

Table 1 Demographics stratified by primary outcome

Patients who did not meet primary Patients who did meet primary P-value
outcome (n 5 492) outcome (n 5 135)
....................................................................................................................................................................................................................
Age (years) 62 ± 16 59 ± 17 0.082
Sex (female) 240 (49%) 66 (47%) 0.702
Race 0.023

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White 397 (81%) 103 (76%)
Black 49 (10%) 9 (7%)
Asian 8 (2%) 5 (4%)
Hispanic 19 (4%) 4 (3%)
Other 19 (4%) 14 (11%)
Past medical history
Coronary artery disease, n (%) 68 (14) 16 (12) 0.552
Congestive heart failure, n (%) 37 (8) 10 (7) 0.965
Stroke, n (%) 36 (7) 3 (3) 0.067
Pulmonary hypertension, n (%) 7 (1) 3 (2) 0.455
Asthma, n (%) 61 (12) 8 (6) 0.033
COPD, n (%) 37 (8) 13 (10) 0.423
Active cancer, n (%) 22 (5) 6 (4) 0.989
Prior history of VTE, n (%) 126 (26) 32 (24) 0.651
Risk factors
Family history of VTE, n (%) 45 (9) 23 (17) 0.009
Recent surgery, n (%) 109 (22) 31 (23) 0.842
Recent hospitalization >_3 days, n 131 (27) 38 (28) 0.724
(%)
Recent trauma, n (%) 25 (5) 9 (7) 0.471
Reduced mobility, n (%) 140 (29) 43 (32) 0.442
Smoker, n (%) 178 (36) 48 (36) 0.894

Data are presented as mean ± SD or n (%) where appropriate. ‘Recent’ was defined as within 4 weeks.
OPD, chronic obstructive pulmonary disease; VTE, venous thromboembolism.

TAPSE/PASP, corroborating high degree of consistency in the intra- .. primary endpoint whereas TAPSE and PASP separately showed sig-
..
observer analyses. .. nificantly lower AUC (Figure 3B). We identified a TAPSE/PASP ratio
Patients who experienced the primary outcome had significantly
.. 0.387 (95% CI 0.304–0.425) as the optimal value for predicting out-
..
lower TAPSE, higher TRV and higher PASP, larger IVC, and more fre- .. come in PE based on the ROC.
quently septal bowing and McConnell’s sign. They also had a lower
.. In multivariate analysis, TAPSE/PASP was independently associated
..
TAPSE/PASP ratio 0.29 (0.21–0.40) compared with those who did .. with primary outcome with an OR 0.026 per unit change (95% CI
not meet the primary outcome [0.47 (0.33–0.70), P < 0.001]. See
.. 0.008–0.080, P < 0.0001). TAPSE and PASP separately were also in-
..
Figure 2. .. dependently associated with the primary endpoint (Table 4).
..
The distribution of the TAPSE/PASP ratio is shown in Figure 3A. .. For secondary outcomes of all-cause mortality, higher TAPSE/
We divided patients into quartiles by TAPSE/PASP ratio (<0.295, .. PASP was associated with lower 7-day all-cause mortality with OR
..
0.295–0.429, 0.430–0.659, >0.659); there was a significant trend asso- .. 0.060 (95% CI 0.007–0.527, P < 0.0001) per unit change. TAPSE, but
ciated with primary outcome (P < 0.0001) across these quartiles. In .. not PASP, predicted 7-day mortality. Only TAPSE/PASP, but not
..
the lowest quartile, 69/158 (44%) of patients experienced adverse .. TAPSE or PASP individually, predicted 30-day all-cause mortality
outcome, compared with; 38/157 (24%), 17/159 (11%), and 11/151 .. with OR 0.326 (95% CI 0.118–0.895, P = 0.0297) per unit change
..
(7%), respectively, in the higher quartiles. .. (Table 4).
.. Figure 4 shows the percentage of events for both primary and the
..
Association with adverse outcome .. two secondary outcomes also stratified by high vs. low TAPSE/PASP
In univariate analysis, TAPSE/PASP were associated with the primary .. with the 0.387 as optimal cut-off. Significantly more events occurred
..
endpoint with an odds ratio (OR) = 0.028 [95% confidence interval .. in the low TAPSE/PASP group during the first 7 days.
(CI) 0.010–0.087, P < 0.0001] per unit change. There was no differ- ..
..
ence between sexes. TAPSE and PASP separately were also associ- .. Sub-analyses
ated with the primary outcome (Table 4). However, in ROC analysis
.. A number of sub-analyses were pre-specified. We believe that the
..
TAPSE/PASP had an AUC of 0.740 (95% CI 0.694–0.787) to predict . primary clinical use of the TAPSE/PASP ratio is in stratifying
The echocardiographic ratio TAPSE/PASP in acute pulmonary embolism 5

Table 2 Clinical PE presentation, stratified by outcome

Patients who did not meet primary Patients who met primary P-Value
outcome (n 5 492) outcome (n 5 135)
....................................................................................................................................................................................................................
Symptoms
Asymptomatic, n (%) 19 (4) 1 (1) 0.093
Dyspnoea, n (%) 364 (74) 96 (71) 0.504

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Chest pain (dull, achy), n (%) 55 (11) 8 (6) 0.072
Chest pain (pleuritic), n (%) 122 (25) 35 (26) 0.789
Syncope, n (%) 43 (9) 20 (15) 0.038
Haemoptysis, n (%) 16 (3) 2 (2) 0.388
Cough, n (%) 85 (17) 25 (19) 0.737
Palpitations, n (%) 45 (9) 10 (7) 0.527
Leg pain, n (%) 91 (19) 20 (15) 0.321
Leg swelling, n (%) 123 (25) 33 (24) 0.895
Vitals and blood analysis
Hypoxia, n (%) 344 (70) 111 (82) 0.005
Highest heart rate, beats/min 105 (90–117) 112 (96–128) <0.001
Lowest systolic blood pressure 118 (102–132) 112 (98–130) 0.084
(mmHg)
Highest respiration rate, breaths/ 20 (20–24) 24 (20–30) <0.001
min
Troponin elevated, n (%) 239 (52) 87 (68) <0.001
NT-proBNP elevated, n (%) 254 (52) 83 (61) 0.042

Data are presented as median with inter-quartile range or n (%) where appropriate. Hypoxia is defined as saturation < 95% on ambient air or need for supplemental oxygen.
PE, pulmonary embolism; PERT, pulmonary embolism response team; NT-proBNP, N-terminal pro b-type natriuretic peptide.

Table 3 Echocardiographic measurements stratified by outcome

Echocardiographic variable Patients who did not meet primary Patients who did meet primary outcome (n 5 135) P-Value
outcome (n 5 492)
....................................................................................................................................................................................................................
TAPSE (mm) 16.9 (13.3–21.0) 13.4 (9.3–16.6) <0.001
TRV (cm/s) 2.7 (2.3–3.1) 2.9 (2.6–3.2) <0.001
RA–RV pressure gradient (mmHg) 28.7 (21.5–37.5) 33.4 (26.8–41.7) <0.001
PASP (mmHg) 34.1 (25.7–44.2) 40.7 (32.7–51.6) <0.001
IVC (cm) 1.7 (1.4–2.1) 2.0 (1.6–2.3) <0.001
TAPSE/PASP (mm/mmHg) 0.47 (0.33–0.70) 0.29 (0.21–0.40) <0.001
McConnell sign present 113 (23%) 61 (45%) <0.001
Septal bowing 128 (26%) 71 (53%) <0.001

Data are presented as median and inter-quartile range.

IVC, inferior vena cava; PASP, pulmonary arterial systolic pressure; RA–RV, right atrial to right ventricular; TAPSE, tricuspid annular plane systolic excursion; TRV, tricuspid
regurgitant velocity.

intermediate-risk PE patients, as high risk-patients with hypotension

.. CI 0.009–0.125, P < 0.0001). Similarly, when excluding hypotensive
..
or arrest would be treated expeditiously, while conversely, few low- .. patients but adjusting for other echocardiographic findings (presence
..
risk PE patients require PERT activations. When excluding high-risk .. of septal bowing, McConnell sign or, RV/LV > 1), the prediction of
patients defined by presentation systemic systolic blood pressure .. the TAPSE/PASP ratio was largely unaffected (OR 0.069, 95% CI
..
<90 mmHg (n = 105), the OR point estimate was largely unaffected .. 0.021–0.227, P < 0.0001).
(OR 0.042, 95% CI 0.014–0.132, P < 0.0001). We then adjusted for .. We aimed to ensure that TAPSE/PASP predicted actual outcome
..
elevated biomarkers in this subgroup and found TAPSE/PASP ratio .. and not PERT-related clinical decision-making in this registry.
was still highly associated with the primary outcome (OR 0.034, 95% .. Accordingly, after excluding from the primary outcome those
..
6 M.D. Lyhne et al.

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Figure 2 Representative images of low and high TAPSE/PASP ratio. Same patient with a TAPSE of 24.3 mm (A) and low TRV of 1.66 m/s (B). With
an estimated RAP of 3 mmHg, the calculated PASP is 14.1 mmHg yielding a TAPSE/PASP ratio of 1.72 mm/mmHg. Another patient with TAPSE
12.8 mm (C), TRV 3.11 m/s (D), and PASP of 53.6 mmHg. The TAPSE/PASP ratio is decreased to 0.24 mm/mmHg as marker of uncoupling. PASP, pul-
monary arterial systolic pressure; RAP, right atrial pressure; TAPSE, tricuspid annular plane systolic excursion; TRV, tricuspid regurgitation velocity.

patients who received thrombus-reducing interventions, 72 clinical

..
.. Combining RV function and RV afterload
outcomes (death, intubation, or need for vasopressors) remained.
TAPSE/PASP also predicted this clinical composite outcome (OR
0.056, 95% CI 0.015–0.209, P < 0.0001), with AUC 0.704 (95% CI
0.639–0.768); however, this was not statistically significantly better
than TAPSE alone (AUC 0.667, 95% CI 0.596–0.739, P = 0.08).
Finally, to make sure that intubation with increased intra-thoracic
pressure did not affect IVC diameter and collapsibility, we excluded
patients intubated at the time of echocardiogram (n = 18) with no ef-
fect on results (OR = 0.029, 95% CI 0.009–0.091, P < 0.0001).
Discussion
This study is the first to show that the echocardiographic index
TAPSE/PASP—a method to integrate estimates of RV function rela-
tive to RV afterload—is independently associated with adverse PE-
related outcome. This ratio is a stronger predictor for adverse out-
come than either of the two parameters separately and is a strong
predictor of adverse outcomes in intermediate-risk PE patients, even
when adjusting for elevated biomarkers or other echocardiographic
findings of RV dysfunction.
.. Risk stratification is critical in acute PE to determine which patients
..
.. are at risk for haemodynamic decompensation and thus may merit in-
.. vasive therapy.2,12 Prior attempts at PE risk stratification have focused
..
.. on an isolated parameter, like RV/LV ratio on CTPA or TTE,9,27,28 or
.. 29–32
.. regional or global RV dysfunction on TTE. Those measures have
.. a restricted focus on the RV consequences without accounting for
..
.. the ambient RV afterload. Yet, others focused on the pulmonary cir-
.. culation characteristics, for example, early systolic notching in the
..
... pulmonary artery33Doppler in PE due to pulmonary obstruction and
.. vasoconstriction, without assessing RV function. Failure to consider
.. the RV–PA unit as a whole may explain why a number of studies of
..
.. potential imaging prognostic measures in PE did not robustly predict
.. outcome.13,34,35
..
.. The importance of jointly analysing RV function and the pulmonary
.. circuit as a unit, as done via the TAPSE/PASP ratio, has been empha-
..
.. sized.15,36 The TAPSE/PASP has normal values in the range 0.8–1.8
.. that may vary with higher ages but not with gender.36–38 Similarly, we
..
.. did not see difference between sexes in a disease state.36 A high ratio
.. means the RV is functioning well given the afterload. The ratio will de-
..
.. crease as PASP increases, when RV function estimated by TAPSE
.. declines, or both. We speculate if changes in PASP is the main
The echocardiographic ratio TAPSE/PASP in acute pulmonary embolism 7

A B

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Figure 3 Histogram and ROC curve of the TAPSE/PASP ratio. (A) Distribution of the TAPSE/PASP ratio in this PE population. (B) ROC curves.
TAPSE/PASP had an AUC of 0.740 (95% CI 0.694–0.787) to predict primary endpoint whereas TAPSE and PASP separately showed significantly lower
AUC in the prediction of adverse outcome (TAPSE AUC 0.698, 95% CI 0.647–0.748, P = 0.017 vs. TAPSE/PASP and PASP AUC 0.646, 95% CI 0.596–
0.695, P < 0.0001 vs. TAPSE/PASP). AUC, area under the curve; PASP, pulmonary arterial systolic pressure; PE, pulmonary embolism; ROC, receiver
operating characteristic; TAPSE, tricuspid annular plane systolic excursion.

..
..
..
Table 4 Correlation between echocardiographic esti- ..
mates of RV function and afterload and the endpoints ..
..
Correlation to primary, com- OR 95% CI P-value
..
..
posite outcome ..
................................................................................................. ..
TAPSE (univariate) 0.878 0.844–0.913 <0.0001 ..
..
PASP (univariate) 1.033 1.020–1.047 <0.0001 ..
TAPSE/PASP (univariate) 0.028 0.010–0.087 <0.0001 ..
..
TAPSE (multivariate) 0.873 0.838–0.910 <0.0001 ..
PASP (multivariate) 1.034 1.020–1.048 <0.0001
..
..
TAPSE/PASP (multivariate) 0.026 0.008–0.080 <0.0001 ..
Correlation (univariate) to 7 days
..
..
all-cause mortality ..
TAPSE 0.901 0.835–0.974 0.0082
..
..
PASP 1.018 0.992–1.044 0.1780 ..
TAPSE/PASP 0.060 0.007–0.527 <0.0001
..
..
Correlation (univariate) to 30 days ..
..
all-cause mortality ..
TAPSE 0.955 0.909–1.005 0.0744 .. Figure 4 Adverse events stratified by TAPSE/PASP ratio.
.. Percentage of events for both primary 7 days composite outcome
PASP 1.009 0.991–1.027 0.3322 ..
TAPSE/PASP 0.326 0.118–0.895 0.0297 .. and the secondary outcomes of 7 and 30 days mortality.
.. Stratification by TAPSE/PASP<0.387 vs. >_0.387 shows significantly
..
All ORs calculated per unit change, i.e. per mm increase for TAPSE; per mmHg .. more adverse events in the low TAPSE/PASP group. PASP, pulmon-
increase for PASP, and per mm/mmHg increase for TAPSE/PASP. .. ary arterial systolic pressure; TAPSE, tricuspid annular plane systolic
CI, confidence interval; OR, odds ratio; PASP, pulmonary arterial systolic pres- .. excursion.
sure; TAPSE, tricuspid annular plane systolic excursion. ..
..
8 M.D. Lyhne et al.
..
determinant in TAPSE/PASP changes, as afterload is the most dynam-
ic factor compared with contractility in the time following acute
intermediate-risk PE in an animal model.39 TAPSE/PASP ratio is not a
measure of function but rather a proxy for VA-coupling (see
below),36 noting TAPSE does not account for ventricular force or
contractility as it does not contain information on ventricular mass or
a time consideration (e.g. acceleration). Despite these potential con-
cerns, the ratio has been shown valuable in pulmonary hypertension,
tricuspid regurgitation, and LV dysfunction.16–18,20,22,40,41 This analysis
now extends the ratio to acute PE.
The combination of RV function and afterload in acute PE has been
investigated in a smaller European cohort which showed promising
results though the ratio was derived in a reciprocal manner.42 Our
cohort differs from that cohort in the proportion of patients with
higher risk PE, and in the specific metric to assess the RV–PA unit.
In chronically progressive pulmonary hypertension, TAPSE/PASP
values were decreased even to lower values than we report in acute
PE.23,24 Lower values of TAPSE/PASP observed in chronic pulmonary
hypertension compared with acute PE might be explained by slower
disease development where the RV has an opportunity to adapt,15
and ultimately PASP can reach very high levels yielding a low ratio.
Another study found the TAPSE/PASP ratio was reduced in systemic
hypertension patients with normal LV function, possibly suggesting
increased pulmonary pressures as an early signal of RV impact even
of a systemic disease.43
Our findings suggest that poor outcomes in PE may be heralded by
a mismatch between RV function and an acute PE-related vascular
load manifested by a TAPSE/PASP ratio <0.4. The effect of this mis-
match can vary depending on the speed of disease progression, as
well as prior RV comorbidities that may generate pulmonary hyper-
tension and RV compensation.
TAPSE/PASP vs. invasive measurements
For all these analyses, it must be recognized that TAPSE is only an es-
timate of RV contractility, specifically the longitudinal contraction of
the RV basal myocardium, and this may not reflect the global state of
RV contraction or characterize specific regional heterogeneity of RV
function. Overall ventricular contraction is, however, mostly longitu-
dinal in the RV6 which is captured by TAPSE. Analogously, PASP is
only an estimate of RV afterload, not necessarily integrating load-
dependencies or changes in flow patterns, vascular adaptabilities, and
impedance.4,44 A more thorough investigation of RV contractility and
RV afterload would require pressure–volume loop recordings to de-
fine the end-systolic pressure–volume relationship (Ees) as the inde-
pendent measure of contractility and the arterial elastance (Ea) as the
afterload. The combination Ees/Ea reflects ventriculo–arterial cou-
pling, and describes if the force of the ventricle matches the afterload
faced.6,44 RV afterload can be estimated by other means, for example
pulmonary vascular resistance or Ea, though both require additional
and more advanced measurements with uncertain assumptions in a
non-invasive setup as an echocardiographic examination.45,46 Further
research is needed to investigate whether such methods improve
risk stratification further without limiting feasibility.
PE can induce RV–PA uncoupling, but in practice, pressure–vol-
ume loop measurements are invasive, expensive, rarely available, and
thus not clinically relevant in acute settings. Accordingly, the TAPSE/
PASP ratio may be used as the echocardiographic counterpart to the
.. RV–PA coupling.43 TAPSE/PASP has been shown to correlate with
.. actual RV–PA coupling18 and to correlate with invasively measured
..
.. RAP, pulmonary vascular resistance, and LV end-diastolic pressure.22
..
..
.. Clinical implementation
.. The TAPSE/PASP ratio could be implemented in near real-time acute
..
.. clinical risk stratification systems as echocardiography is easy to per-
.. form, inexpensive, harmless, and widely available. Even in supine,
..
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.. critically-ill patients that cannot co-operate with standard TTE posi-
.. tioning, IVC, TRV, and TAPSE can be measured in subcostal views
..
.. enabling measurement of RV function.47,48
.. We have retrospectively established TAPSE/PASP ratio cut-off of
..
.. 0.4 to identify PE patients at risk of deterioration. This is comparable
.. with an optimal TAPSE/PASP cut-off of 0.49 in moderate-severe tri-
..
.. cuspid regurgitation as recently suggested.40 A prospective study
..
.. should be designed to investigate efficacy of this cut-off to trigger
.. more aggressive management of patients with acute PE. Further re-
..
.. search is also warranted to investigate the TAPSE/PASP ratio in a
.. larger, unselected PE population and to assess if the ratio is suitable
..
.. for long-term prognosis or in prediction of chronic thromboembolic
.. pulmonary hypertension.
..
..
.. Limitations
..
.. This study analysed a large population of acute PE patients from a
.. prospective cohort with robust clinical correlates and well-
..
.. phenotyped patients with complete data ascertainment. However,
.. the present study has limitations. Because we analysed a registry of
..
.. mostly intermediate- and high-risk PE patients at a single institution,
..
.. generalizability may be limited. However, institutional practice sug-
.. gests nearly all patients with intermediate- or high-risk PE patients
..
.. are treated by the PERT team, and the sample size is large. Secondly,
.. the metrics of RV–PA coupling are not invasively derived, but rather
..
.. echocardiographic, relying on known correlation between the
.. TAPSE/PASP ratio and invasive measurements.18 Echocardiographic
..
.. metrics of RV function have limitations. TAPSE is a common estimate
.. of RV function, but it measures longitudinal RV function; additionally,
..
.. longitudinal RV function may differ from radial or apical RV contractil-
.. ity in certain disease states. Accordingly, TAPSE does not reflect
..
.. overall RV function. We did not record visual, qualitative estimate of
.. RV function, which might introduce higher degree of inter-observer
..
.. variability and therefore would depend on echocardiographer ex-
..
.. perience. The TAPSE/PASP ratio is a simple, quantitative metric to
.. augment reproducibility. Thirdly, TTE was performed within two
..
.. days of PERT activation but not necessarily at the exact hour of acute
.. PE presentation or diagnosis. Lastly, some high-risk PE patients were
..
.. excluded because they received rescue therapies prior to an echo-
.. cardiogram. However, these patients were likely to have had RV–PA
..
.. dysfunction and exclusion of these patients would be expected to
.. bias the result towards the null hypothesis.
..
..
..
..
.. Conclusion
..
.. We demonstrate that a combination of RV function and pulmonary
..
.. pressure, estimated by the echocardiographic ratio TAPSE/PASP,
.. improves prediction of adverse short-term outcome in patients with
..
. acute non-low-risk PE. External validation of the ratio, and its
The echocardiographic ratio TAPSE/PASP in acute pulmonary embolism 9

.. 13. Barrios D, Morillo R, Lobo JL, Nieto R, Jaureguizar A, Portillo AK et al.

performance characteristics as embedded into a prospective ..
decision-analysis strategy in acute PE is warranted. .. Assessment of right ventricular function in acute pulmonary embolism. Am Heart
.. J 2017;185:123–9.
.. 14. Sanchez O, Trinquart L, Colombet I, Durieux P, Huisman MV, Chatellier G et al.
Acknowledgements .. Prognostic value of right ventricular dysfunction in patients with haemodynamic-
Thank you to the research staff at Centre for Vascular Emergencies
.. ally stable pulmonary embolism: a systematic review. Eur Heart J 2008;29:
..
for help and support. Icons for the visual abstract are from .. 1569–77.
.. 15. Vonk Noordegraaf A, Haddad F, Chin KM, Forfia PR, Kawut SM, Lumens J et al.
flaticon.com. .. Right heart adaptation to pulmonary arterial hypertension: physiology and patho-
.. biology. J Am Coll Cardiol 2013;62:D22–33.
Funding ..

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16. Bragança B, Trêpa M, Santos R, Silveira I, Fontes-Oliveira M, Sousa MJ et al.
.. Echocardiographic assessment of right ventriculo-arterial coupling: clinical corre-
M.D.L. receives scholarship from Aarhus University, Denmark. The fol- ..
lowing foundations for the support of M.D.L.’s research tenure in Boston: .. lates and prognostic impact in heart failure patients undergoing cardiac resynch-
.. ronization therapy. J Cardiovasc Imaging 2020;28:109–20.
Eva and Henry Fraenkel Memorial Foundation, AP Moeller Foundation, .. 17. Guazzi M, Bandera F, Pelissero G, Castelvecchio S, Menicanti L, Ghio S et al.
Aarhus University, Denmark-America Foundation, Reinholdt W. Jorcks .. Tricuspid annular plane systolic excursion and pulmonary arterial systolic pres-
Foundation, Knud Hoejgaards Foundation, Lundbeckfonden, and Family
.. sure relationship in heart failure: an index of right ventricular contractile function
.. and prognosis. Am J Physiol Heart Circ Physiol 2013;305:H1373–81.
Hede Nielsen Foundation. ..
.. 18. Guazzi M, Dixon D, Labate V, Beussink-Nelson L, Bandera F, Cuttica MJ et al. RV
Conflict of interest: C.K. discloses grant funding to his institution .. contractile function and its coupling to pulmonary circulation in heart failure
.. with preserved ejection fraction: stratification of clinical phenotypes and out-
from Janssen, Diagnostica Stago, Siemens Healthcare Diagnostics and con- .. comes. JACC Cardiovasc Imaging 2017;10:1211–21.
sulting agreements with Boston Scientific and EKOS corporation. The .. 19. Sultan I, Cardounel A, Abdelkarim I, Kilic A, Althouse AD, Sharbaugh MS et al.
remaining authors have nothing to disclose.
.. Right ventricle to pulmonary artery coupling in patients undergoing transcatheter
..
.. aortic valve implantation. Heart 2019;105:117–21.
.. 20. Gorter TM, van Veldhuisen DJ, Voors AA, Hummel YM, Lam CSP, Berger RMF
.. et al. Right ventricular–vascular coupling in heart failure with preserved ejection
Data availability .. fraction and pre- vs. post-capillary pulmonary hypertension. Eur Heart J
.. Cardiovasc Imaging 2018;19:425–32.
The data underlying this article will be shared on reasonable request
.. 21. Martens P, Verbrugge FH, Bertrand PB, Verhaert D, Vandervoort P, Dupont M
..
to the corresponding author. .. et al. Effect of cardiac resynchronization therapy on exercise-induced pulmonary
.. hypertension and right ventricular–arterial coupling. Circ Cardiovasc Imaging 2018;
.. 11:e007813.
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