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Detection and Characterization of Intracardiac Thrombi on MR Imaging

¹ Department of Diagnostic and Interventional Radiology, University Hospital Essen, Hufelandstraße 55, D-45122 Essen, Germany.
² Department of Cardiology, University Hospital Essen, D-45122 Essen, Germany.
³ Department of Cardiology, Elisabeth Hospital Essen, D-45138 Essen, Germany.

Received April 5, 2002; accepted after revision May 17, 2002.
Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. The aim of our study was to compare the diagnostic accuracy achieved using different MR techniques with the diagnostic accuracy achieved using transthoracic and transesophageal echocardiography to detect intracardiac thrombi.

MATERIALS AND METHODS. Twenty-four patients with known or suspected intracardiac thrombi were examined using MR imaging and echocardiography. All MR examinations were performed on a 1.5-T MR scanner using dark-blood—prepared half-Fourier acquisition single-shot turbo spin-echo (HASTE) sequences, fast imaging steady-state free precession (trueFISP) cine sequences, and inversion recovery gradient-echo fast low-angle-shot (inversion recovery turbo FLASH) sequences after injection of 0.2 mmol/kg of gadolinium diethylene triamine pentaacetic acid.

RESULTS. MR imaging and echocardiography revealed 12 thrombi—two in the right atrium, one in the right ventricle, three in the left atrium, and six in the left ventricle. Compared with echocardiography, MR imaging revealed three additional thrombi in the left ventricle; these thrombi were confirmed at surgery. All 15 thrombi appeared as filling defects on early contrast-enhanced inversion recovery turbo FLASH MR images. Only seven thrombi were detected on HASTE images, and 10 thrombi were seen on trueFISP images. Four thrombi showed enhancement 10-20 min after contrast material injection and were characterized as organized clots.

CONCLUSION. Contrast-enhanced inversion recovery turbo FLASH sequences were superior to dark-blood—prepared HASTE and trueFISP cine MR images in revealing intracardiac thrombi. Compared with transthoracic echocardiography, MR imaging was more sensitive for the detection of left ventricular thrombi. The characterization of thrombi may be used to predict the risk of embolism, which is higher for subacute clots than for organized thrombi.

Introduction

Top Abstract Introduction Materials and Methods Results Discussion References

 
Thrombi of the chambers of the left heart are a common source of stroke and other arterial embolic syndromes. Thrombi of the right heart are frequently detected in patients with pulmonary embolism [1, 2]. In clinical practice, transthoracic echocardiography is the diagnostic tool of first choice in these patients. However, the inability to visualize all cardiac chambers and the reduced image quality in patients who are not well suited for the procedure are major limitations of transthoracic echocardiography. Therefore, transesophageal echocardiography has emerged as the most sensitive technique for the detection of intracardiac thrombi and is believed to be the single best test for patients with suspected intracardiac thrombi [3].

However, distinguishing normal myocardium from clots may be difficult on echocardiography, hampering the diagnosis of thin mural thrombi. In addition, because of the lack of diagnostic criteria, differentiating subacute thrombi from organized thrombi on echocardiography—a distinction that is important in predicting the risk of embolic complications [4]—is challenging.

Within the last 10 years, MR imaging has emerged as a new noninvasive cardiac imaging technique that can provide complementary information to the data obtained by echocardiography in patients with various cardiac diseases. MR imaging can be considered the first-line imaging technique in patients with congenital heart disease and in those with suspected cardiac tumors. Recently, several new cardiac MR techniques have been introduced to improve spatial and temporal resolution, robustness, and contrast properties [5, 6] of the modality. These rapid technical developments have expanded the indications for cardiac MR imaging.

The aim of our study was to evaluate the diagnostic accuracy achieved with different unenhanced and contrast-enhanced MR sequences for the detection of intracardiac thrombi and to compare the results with those achieved using transthoracic and transesophageal echocardiography.

Materials and Methods

Top Abstract Introduction Materials and Methods Results Discussion References

 
After giving informed consent, 24 consecutive patients (17 men and seven women; age range, 23-76 years; mean age ± SD, 57 ± 14 years) who had been referred to the echocardiography laboratory for evaluation of known or suspected intracardiac thrombi were enrolled in our study, which was performed in accordance with regulations set forth by the local institutional review board. Transthoracic echocardiography was performed in all patients, and transesophageal echocardiography was performed in 11 of 24 patients with suspected atrial thrombi. Two-dimensional (2D) echocardiographic examinations were performed with state-of-the-art machines using standard views and techniques in accordance with the guidelines of the American Society of Echocardiography. Images were obtained with patients in the left lateral position at end-expiration by experienced cardiologists.

A 1.5-T scanner (Magnetom Sonata; Siemens Medical Solutions, Erlangen, Germany) was used for all MR imaging. The MR imaging protocol included an ECG-triggered dark-blood—prepared half-Fourier acquisition single-shot turbo spin-echo (HASTE) sequence (TR/TE, 2 heartbeats/60 msec; flip angle, 160°) covering the entire heart in the axial orientation. Thereafter, four-chamber and two-chamber views as well as contiguous short-axis images of the entire heart were acquired with a fast imaging steady-state free precession (trueFISP) cine sequence (3 msec/1.5 msec; flip angle, 60°). Images in the oblique orientation were obtained to further investigate suspicious areas.

Immediately after the injection of 0.2 mmol/kg of gadolinium diethylene triamine pentaacetic acid (Magnevist; Schering, Berlin, Germany) (flow rate, 2 mL/sec), breath-hold ECG-triggered 2D inversion recovery turbo FLASH images (8/4; flip angle, 25°) of four- and two-chamber views of the heart were acquired. Repeated three-dimensional (3D) inversion recovery turbo FLASH sequences (4/1.4; flip angle, 10°) in the short-axis orientation were then performed. In patients with suspicious findings, additional oblique slices were obtained, using either the 2D or the 3D inversion recovery turbo FLASH sequence. Images were acquired both immediately after injection of the contrast material and as long as 20 min after the injection. To optimize the image contrast, we varied the inversion time (nonselective inversion pulse) for both sequences between 180 and 300 msec.

The typical in-plane resolution was 1.6 x 1.3 mm² for both sequences. Whereas the 2D sequence is a single-slice technique (slice thickness, 8 mm), the 3D sequence can acquire as many as 24 slices with a slice thickness of 4 mm in one breath-hold of reasonable length, using a shorter TR, partial Fourier reconstruction (6/8), z-axis interpolation, and longer data acquisition window, with 77 k-space lines per heartbeat to improve speed. The total imaging time required, including patient positioning, was 45-60 min.

All MR images were interpreted by consensus by two experienced radiologists who were unaware of the diagnosis and of the results of the echocardiographic examinations. Hard copies were used for the interpretation of the HASTE and inversion recovery turbo FLASH images, whereas the trueFISP images were reviewed as cine loops on a workstation. The interpretations for the HASTE, trueFISP, and inversion recovery turbo FLASH MR images were performed separately.

Results

Top Abstract Introduction Materials and Methods Results Discussion References

 
Echocardiography revealed 12 intracardiac thrombi. The thrombi were located in the right atrium (n = 2), right ventricle (n = 1), left atrium (n = 3), and left ventricle (n = 6). One thrombus in the appendage of the right atrium and two of the thrombi in the left atrium were visualized only on transesophageal, not on transthoracic, echocardiography. All thrombi seen on echocardiography were detected on MR imaging (Table 1). Cardiac MR imaging revealed three additional thrombi in the left ventricle not seen on transthoracic echocardiography. None of these three patients had undergone transesophageal echocardiography. Therefore, cardiac MR imaging revealed 15 thrombi in 24 patients. In seven patients, including the three with discrepant findings, the MR imaging diagnosis was confirmed at surgery.

The thrombi appeared isointense or slightly hyperintense relative to the myocardium on dark-blood—prepared HASTE images (Fig. 1A). Both of the right atrial thrombi, one of the left atrial thrombi, and four of nine left ventricular thrombi were detectable on HASTE images. The other eight thrombi were not visible on HASTE images because of poor contrast between the thrombus and the myocardium and because of slow-flow artifacts, which hampered the establishment of the correct diagnosis, especially in patients with impaired ventricular function or left ventricular aneurysms (Fig. 2C).

View larger version (129K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —28-year-old man with myocarditis and thrombus (arrow, A—C) in right atrial appendage. Axial dark-blood—prepared HASTE MR image shows mass in right atrial appendage isointense relative to myocardium.

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —58-year-old man who had myocardial infarction 6 weeks before imaging. Axial dark-blood—prepared HASTE image reveals bright signal in left ventricular apex caused by slow flow.

Thrombi showed low signal intensity on trueFISP cine images (Figs. 1B, 3A, 4A, and 4B). Therefore, the differentiation of the myocardium from the thin mural thrombus was not possible on trueFISP images (Figs. 2A, 2B, 4A, and 4B). Both right atrial thrombi, the only right ventricular thrombus (Fig. 3A), two left atrial thrombi, and five of the nine left ventricular thrombi were detectable on trueFISP images.

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —28-year-old man with myocarditis and thrombus (arrow, A—C) in right atrial appendage. Diastolic fast imaging steady-state free precession cine MR image obtained in short axis shows mass in right atrial appendage hypointense relative to blood.

View larger version (123K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —32-year-old woman with deep vein thrombosis and pulmonary embolism. Diastolic fast imaging steady-state free precession cine MR image obtained in short axis reveals low-signal-intensity mass (arrow) in right ventricular cavity, indicating right ventricular thrombus (pulmonary emboli in transit).

View larger version (125K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —63-year-old man who had myocardial infarction 4 months before imaging. Two-chamber-view diastolic (A) and systolic (B) cine MR images obtained with fast imaging steady-state free precession (trueFISP) sequence reveal akinetic apical left ventricular wall. Differentiation of myocardium and mural thrombus is unfeasible on trueFISP images.

View larger version (137K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —63-year-old man who had myocardial infarction 4 months before imaging. Two-chamber-view diastolic (A) and systolic (B) cine MR images obtained with fast imaging steady-state free precession (trueFISP) sequence reveal akinetic apical left ventricular wall. Differentiation of myocardium and mural thrombus is unfeasible on trueFISP images.

View larger version (142K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —58-year-old man who had myocardial infarction 6 weeks before imaging. Four-chamber-view diastolic (A) and systolic (B) cine MR images obtained with fast imaging steady-state free precession sequence show lack of systolic wall thickening (arrow).

View larger version (144K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —58-year-old man who had myocardial infarction 6 weeks before imaging. Four-chamber-view diastolic (A) and systolic (B) cine MR images obtained with fast imaging steady-state free precession sequence show lack of systolic wall thickening (arrow).

Delineation of thrombi was optimal on early contrast-enhanced inversion recovery turbo FLASH images. All thrombi appeared as lowsignal-intensity filling defects in the cavity. Four of 15 thrombi showed significant contrast enhancement 10-20 min after the injection of contrast material (Fig. 4D).

View larger version (111K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4D. —63-year-old man who had myocardial infarction 4 months before imaging. Two-chamber late contrast-enhanced 2D inversion recovery turbo FLASH image clearly reveals area of hyperenhancement (indicating myocardial scar tissue). Thrombus shows significant contrast enhancement.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The ECG-triggered 3D inversion recovery turbo FLASH sequence provided excellent contrast and high spatial resolution after the administration of an extracellular contrast agent, making this technique the most accurate to use for the detection of intracardiac thrombi. The 3D sequence allows full cardiac coverage in a single breath-hold and was shown to be well suited for revealing and characterizing intracardiac thrombi.

Among the imaging techniques routinely used to visualize intracardiac thrombi, 2D transthoracic echocardiography is the modality of first choice. Reasons include availability, high accuracy, and low cost. The technique is characterized by sensitivity and specificity values for left ventricular thrombi of approximately 90% compared with aneurysmectomy or autopsy [7]. Several studies have shown transesophageal echocardiography to be more sensitive for the detection of atrial thrombi than transthoracic echocardiography [3, 8], particularly for the detection of thrombi in the left atrial appendage. However, transesophageal echocardiography is semiinvasive. The sensitivity of angiocardiography for the detection of intracardiac thrombus is unacceptably low, and indium-111 platelet scanning is time-consuming and expensive [7]. Contrast-enhanced CT is more sensitive for ventricular and atrial thrombi than is transthoracic echocardiography, but the technique has been shown to be inferior to transesophageal echocardiography for revealing atrial thrombi [9, 10]. These imaging techniques are of limited use in distinguishing between a thrombus and a cardiac tumor or in characterizing a thrombus as acute or subacute.,

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —32-year-old woman with deep vein thrombosis and pulmonary embolism. In contrast-enhanced two-dimensional inversion recovery gradient-echo fast low-angle-shot MR image obtained in short axis, mass (arrow) does not show contrast enhancement.

View larger version (115K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —32-year-old woman with deep vein thrombosis and pulmonary embolism. Posterior-view maximum-intensity-projection angiogram of pulmonary artery shows occlusion (arrow) of left posterior basal segment artery.

Over the years, cardiac MR imaging with different types of sequences has emerged as a noninvasive alternative for the detection and characterization of intracardiac masses [11,12,13,14]. In agreement with earlier studies, our data show that the value of spin-echo and turbo spin-echo MR imaging sequences for revealing intracardiac masses is limited by artifacts caused by slow-flowing blood [11, 15]. Because of the high signal intensity inherent to blood, gradient-echo sequences are robust and more sensitive for the detection of intracardiac thrombi. The differentiation of a mural thrombus from the myocardium can be challenging, however [11]. The recently developed trueFISP sequence used in our study improves the contrast between the myocardium and blood [6], but thrombi are isointense relative to the myocardium, so the diagnosis of mural thrombi may be hampered.

The IV administration of gadolinium diethylene triamine pentaacetic acid was shown to enhance the contrast between the myocardium and thrombi, thereby improving our ability to detect and characterize thrombi [4, 14]. Our data suggest an ECG-triggered inversion recovery turbo FLASH sequence originally developed for imaging myocardial infarction [5] is optimally suited for imaging cardiac thrombi also. Immediately after the injection of contrast material, the myocardium and the cardiac cavity show high signal intensities that allow easy detection of cardiac thrombi (Fig. 2A,2B,2C,2D). Inversion times can be varied to improve the contrast between thrombi and the myocardium. The signal intensity of myocardial infarctions, which are frequently associated with left ventricular thrombi, increases over time, permitting easy differentiation between nonviable infarcted tissue and subacute thrombi (Fig. 1A,1B,1C). A recently developed ECG-triggered 3D inversion recovery turbo FLASH sequence even allows full cardiac coverage in a single breath-hold and seems ideally suited for the detection of intracardiac thrombi. However, use of ECG triggering is a prerequisite for obtaining high-quality images. Although not present in our study, artifacts may occur in patients with atrial fibrillation or other arrhythmias, which are frequently associated with intracardiac thrombi.

View larger version (113K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2D. —58-year-old man who had myocardial infarction 6 weeks before imaging. Four-chamber-view late contrast-enhanced two-dimensional inversion recovery gradient-echo fast low-angle-shot MR image reveals area of hyperenhancement, indicating myocardial scar tissue. Arrowhead indicates thin mural thrombus that was not detectable on echocardiography.

View larger version (130K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —28-year-old man with myocarditis and thrombus (arrow, A—C) in right atrial appendage. Early contrast-enhanced three-dimensional inversion recovery gradient-echo fast low-angle-shot MR image obtained in short axis reveals filling defect in right atrial appendage.

Intracardiac thrombi are associated with a variety of diseases. Functional disorders such as myocardial infarction or atrial fibrillation are a common cause of cardiac thrombi [7, 16]. The frequency of left ventricular thrombi is approximately 30% in patients with an acute or healed myocardial infarction. Most thrombi develop within the first week after the infarction and are most often noted at the apex of the left ventricle in patients who have had an anterior myocardial infarction [7]. Deep vein thrombosis or the use of central venous catheters may lead to development of thrombi in the right heart, which should be considered pulmonary emboli in transit [1, 17,18,19]. Chronic anabolic steroid abuse as well as several disorders and diseases such as Behçet's syndrome, coagulopathies, Löffler's endocarditis, Churg-Strauss syndrome, or right atrial aneurysm should be considered potential causes of intracardiac thrombi [20,21,22,23,24]. In these rare clinical settings, the differentiation between thrombi and cardiac tumors can be challenging [21, 24], and MR imaging may provide additional information to that obtained from echocardiography.

Intracardiac thrombi may cause arterial or pulmonary embolisms and should be regarded as life-threatening. It is estimated that in approximately 30% of cases of cerebral infarction, the causative thrombus originated in the heart [2, 3]. Cardiac diseases or abnormalities that may cause arterial emboli include atrial and ventricular thrombosis, cardiac tumors, thrombosis on heart valve prostheses, and endocarditis [8]. Our data indicate that contrast-enhanced MR imaging depicts intracardiac thrombi more accurately than transthoracic echocardiography does and—in a limited number of cases—is as sensitive as transesophageal echocardiography. Cardiac MR imaging is the most accurate imaging modality in patients with suspected cardiac tumors. However, cardiac MR imaging cannot replace echocardiography in patients who have had a cerebral stroke because endocarditis, thrombosis on heart valve prostheses, and other potential sources of embolism—patent foramen ovale, valve strands, atrial septum aneurysm, and dystrophy of mitral annulus—are difficult to visualize on MR imaging.

View larger version (113K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —63-year-old man who had myocardial infarction 4 months before imaging. In two-chamber early contrast-enhanced two-dimensional (2D) inversion recovery gradient-echo fast low-angle-shot (turbo FLASH) image, thrombus (arrow) appears as filling defect in cavity with low signal intensity.

In patients with a pulmonary embolism, the rare finding of right heart thrombi may be underdiagnosed. Clinical studies using echocardiography and autopsy studies suggest that these thrombi occur in 6-18% of patients with a pulmonary embolism [25,26,27]. Most of these patients cannot undergo MR imaging because they present with severe dyspnea or cardiogenic shock [1, 26]. Transesophageal echocardiography is unquestionably the imaging technique of first choice in these patients. Use of MR imaging should be restricted to clinically stable patients who have either no symptoms or only minor ones and in whom potential differential diagnoses like intracardiac tumors and congenital structures such as Chiari's network or persistent eustachian or thebesian valves cannot be excluded with certainty. In addition, cardiac MR imaging may be combined with pulmonary MR angiography [28] to provide a single test for the pulmonary vasculature and heart in patients with suspected pulmonary embolism.

The risk of embolism depends on morphologic parameters that can easily be assessed on echocardiography and MR imaging. The embolic risk is approximately 50% for mobile or protruding thrombi compared with an embolic risk of approximately 10% for nonmobile or flat thrombi [7]. MR imaging can distinguish subacute clots—which do not enhance after contrast material injection—from organized thrombi [4]. Four of the 15 thrombi in our study showed significant enhancement and could be considered organized clots. Such characterization provides more information than echocardiography does and may be of great clinical interest because embolic complications are more likely to occur with subacute clots than with organized thrombi.

Echocardiography remains the imaging modality of choice in patients with suspected intracardiac thrombi. However, our data show that ECG-triggered contrast-enhanced cardiac MR imaging is emerging as an accurate noninvasive alternative technique for the detection and characterization of intracardiac thrombi.

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