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Pulmonary Embolism, Systemic and Paradoxical Embolism and Deep Venous Thrombosis

Del Castillo, José Maria; Orlandi Fábio; Capellini Luiz Fernando; Grossmann Rosana; Nakajima Elisa; Hublard Ernesto Luiz; Cortese Marcelo.

Instituto de Cardiologia de São Paulo - Hospital Santa Paula.
São Paulo, Brasil

Material and Methods

Purpose: Research intracardiac anomalous echoes in patients with deep venous thrombosis (DVT) and suspiction of pulmonary embolism (PE) to assess through Transesophageal Echocardiography (TEE) the risk of paradoxical embolism by the observation of the foramen ovale.
Material and Methods: It has been studied through TEE 22 patients with DVT who also had clinical signs of PE, 6 males and 16 females, average age 59 years. It has been researched the presence of echogenic anomalous material in heart cavities and in pulmonary artery and analyzed the foramen ovale to determine its permeability and the membrane's movements.
Results: There were echocardiographic evidence of thrombi in 18 patients in right heart cavities or pulmonary artery. There was an increase of pulmonary pressure in 12 patients and, in 4 patients, there were anomalous echoes in left cavities with signs of paradoxical embolism (permeable foramen ovale with thrombi through the orifice in 2 patients).There was death in 4 cases due to complications of pulmonary embolism and a death due to cerebral embolism.
Discussion: the complications of venous thrombosis of the lower extremities with pulmonary embolism (PE) is a life threatening risk factor. Even in clinically controlled cases , the increase of pulmonary pressure due to pulmonary embolism can provoke paradoxical sistemic embolism through the foramen ovale.
Conclusion: TEE constitutes a very helpful mean to the diagnostic of pulmonary embolism as well as to diagnose and to determinate the possibility of paradoxical sistemic embolism due to right chambers hypertension.


Foreword: Lower extremities deep venous thrombosis forms the third more important cause of cardiovascular morbility in developed countries and presents the potential risk of pulmonary embolism. About 4% of hospital autopsies evidence pulmonary embolism as causa mortis and more then half the number of such patients present deep venous thrombosis of lower extremities. The acute increase of pressure in right cardiac chambers decurrent of pulmonary embolism can make possible the passage of embolic material through pervious foramen ovale making paradoxical embolism possible.

Pulmonary embolism diagnosis is based on pulmonary cintilography, on pulmonary angiography and on laboratory detection of fibrin degradation products.Venous scan duplex is being more and more used to diagnosis venous deep thrombosis and transthoracic and transesophageal echocardiography to detect right cardiac chambers acute increase of pressure signs as well as the presence of embolic material in cavities and in pulmonary artery.


Objectives:  Research through transesophageal echocardiography intracardiac anomalous echoes in patients with deep venous thrombosis of lower extremities. Assess through the increase of pulmonary pressure and foramen ovale membrane motion the paradoxical embolism risk.


Material and Methods:  It has been studied 22 patients with deep venous thrombosis of the lower extremities who presented suggestive clinical signs of pulmonary embolism (thoracic pain or pain with pleural characteristics, dyspnea). Sixteen female and six male patients. The mean of ages was 59 years.

It has been used a HP Sonos 1000 echocardiographic equipment with multiplanar transesophageal 5.0 MHz probe. Oropharyngeal anesthesia with Lidocaine spray 10%. In ICU examinations (16 patients) it has been used unit sedation routine in 11 patients who were in assisted ventilation mode and Midazolam 5mg IV in 3 of 5 remaining patients. In 6 ambulatory patients only 2 needed sedation with IV Midazolam.

All examinations have beeen recorded in VCR tape for subsequent analysis. It has been measured right and left ventricles diameters in transgastric tranverse position at mitral valve leaflets level. It has been estimated, with continous Doppler, right ventricular systolic pressure (representative of pulmonary pressure) through tricuspid regurgitation peak velocity. To the pressure calculation by Doppler formula 10 mmHg has been added. This number (10 mmHg) is the constant pressure value used in our service to represent right atrium pressure (Figure 1) . It also has been calculated the relationship between right and left ventricules diastolic diameter. In patients where thrombotic material has been detected its morphology and location have been described.

For all obtained measures it has been calculated mean and mean standard deviation. To compare the relationship between right and left ventricles diameters it has been used linear regression equation.

No further statistical comparison have achieved due to the non-random sample nature.

Figure 1

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Transesophageal echocardiogram. Left: transgastric transversal approach showing left and right ventricles diameter measures.
Right: Continuous waveDoppler record of the tricuspid regurgitation and pulmonary pressure calculation. VE: left ventricle;
VD: right ventricle; Rel.: right and left ventricular diameter relationship; Vel. Refx. Tric.: tricuspid regurgitation flow
velocity; Pres. pulmonar: systolic pulmonary pressure.


Results: Table 1 shows the summary of echocardiographic findings. In 18 patients embolic intracavity material has been found. Pulmonary pressure has been estimated in 17 patients.

Graph 1 shows the existent correlation between the ventricles diameter and pulmonary pressure relationship . One can notice that as right ventricle diameter rises, pulmonary pressure rises too.

Table 1-Transesophageal ecocardiogram parameters obtained in patients
with deep venous thrombosis of the lower extremities.

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RVDd: right ventricle diastolic diameter; LVDd: left ventricle diastolic diameter; RV/LV: right ventricle-left ventricle diameter relationship; PSP: pulmonary systolic pressure; RA: right atrium; PT: pulmonary main artery; RB: pulmonary artery right branch; LA: left atrium; NV: non-visualized; Mean: aritmetic mean; St. Dev.: mean standard deviation.

Grafic 1

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Linear correlation between righ and left ventricular diameter relationship (Relação VD/VE) and pulmonary systolic pressure (PSTP). r: correlation value; Sx: standard deviation; y=3,5+78*x: regression equation.


Discussion:  According medical literature, venous deep lower extremities thrombosis diagnosis is made in 57% of cases with pulmonary embolism. This emphasizes the importance of the venous circulation of lower extremities investigation through vascular scan duplex, a method more and more divulged, as well as the echodopplercardiographic investigation.

The great number of patients who presented pulmonary embolism evidences observed in this series may be due to studies achieved in patients with strong suspicion of pulmonary embolism or in patients where the diagnosis had already been made.

The main embolic material positioning in cardiovascular cavities was the right pulmonary artery branch, separately or associated to other locations (16 observations), probably due to transesophageal echocardiography easiness to research this branch till bronchial branches origin. No embolism evidence has been observed in left branch, probably due to transesophageal echocardiography difficulty in analyzing this branch which directs posteriorly through pulmonary parenchyma. Pulmonary artery trunk, mainly in the bifurcation area was the second most common embolic material positioning. (11 observations), a fact that was also frequently observed by pathological anatomy (Figure 2). In right ventricular cavity no evidence of embolic material has been found. The right ventricle trabeculation seems to disguise the sight of little thrombi adhered to its walls. Right atrium has shown thrombi in 6 patients, separately or associated to other locations. Such high incidence can be explained by patients’ main disease (deep venous thrombosis) where thrombi fragments migrate through inferior vein cava towards heart whose first found structure is the atrial cavity. Some of these thrombi (4 patients) were adhered to the interatrial septum. In 2 cases the passage of embolic material to left atrium has been observed through foramen ovale. Pulmonary pressure acute increase and, consequently right atrium pressure increase, can explain such fact as they favor fossa ovalis intermittent opening with right to left adressed flow in some moments of the cardiac cycle. The two left atrium observed thrombi were pediculate. Both patients presented cerebral embolism signs and one of them died of such cause (Figure 3) . Other four patients presented intra hospital deaths due to pulmonary embolism complications. In other 3 patients left bulging of fossa ovalis area has been noticed in two cases with intermittent right-to-left flow through foramen ovale (color flow mapping aided analysis) (Figure 4). In four patients no evidence of embolic material in cardiac cavities could have been seen what cannot exclude the pulmonary embolism hypothesis at all, as thrombi can be located out of the ultrassonic beam coverage areas such as the peripheral part of the right pulmonary artery branch, the left pulmonary artery branch or the right ventricular cavity.

Figure 2

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Transesophageal echocardiogram of the main pulmonary artery and its
branches using transversal approach showing thrombi in left lateral wall
of the pulmonary trunk (arrows) and in the bifurcation and origin of the
right pulmonary branch. Ao: aorta; TP: main pulmonary artery; RD:
right branch of the pulmonary artery; RE: left branch of the pulmonary

Figure 3

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Venous scan duplex and transesophageal echocardiogram in patient with deep venous thrombosis and paradoxical embolism. Left: venous scan dupelx of the left leg showing proximal thrombosis of the deep venous system near the saphenofemoral junction. Right: transesophageal echocardiogram showing right atrial thrombi in the lateral wall and interatrial septum and into the left atrium, close to foramen ovale membrane. (pediculate thrombus).
VFC: common femoral vein; VSI: greater saphenous vein; Tr.: thrombus; AE: left atrium; AD: right atrium; VE: left ventricle; VD: right ventricle; FO: foramen ovale.

Figure 4

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Transesophageal ecocardiogram tranversal approach showing right (AD)
and left atria (AE) and tricuspid valve (V.Tr.). The foramen ovale
membrane (Membr. FO) is bulged to the left and right-to-left shunt (Shunt)
is observed across the communication.

In 17 patients pulmonary pressure has been estimated through tricuspid regurgitation flow analysis. In other 5 patients the regurgitation flow was not appropriate to pressure calculation. Pulmonary pressure was increased (systolic pressure greater than 35 mmHg) in 12 patients. Diastolic right ventricle diameter was increased in comparison to the left ventricle diameter in 10 patients (relationship between right and left ventricle diameters greater than 0.6). This rise can have something to do with pulmonary pressure increase as we analyze these two parameters through regression equation (Graph 1). This is important as the right ventricle diameter rise associated to the pulmonary pressure increase can be an indicator of pulmonary embolism in patients with such clinical suspicion.


Conclusions: Transesophageal echocardiography is a great value method to pulmonary embolism diagnosis, either by embolic material direct visualization in cardiac cavities and pulmonary artery or by right ventricle dilatation assessment and pulmonary pressure increase. Foramen ovale area assessment is very important, in patients with pulmonary hypertension where one can detect embolic material passing through the hole or observe membrane bulging with intermittent right-to-left flow above all. Echocardiographic monitorization can decide trombolitic therapeutic or even inferior cava filter placement, a proceeding broadly used in orthopedical surgery and in major trauma treatment.


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