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(Stroke. 1995;26:1820-1824.)
© 1995 American Heart Association, Inc.

Articles

Selection of Patients for Transesophageal Echocardiography After Stroke and Systemic Embolic Events

Role of Transthoracic Echocardiography

Dominic Y. Leung, MBBS, MRCP (UK), FRACP; Ian W. Black, MBBS, FRACP; Gregory B. Cranney, MBBS, FRACP; Warren F. Walsh, MBBS, FRACP; Richard A. Grimm, DO; William J. Stewart, MD James D. Thomas, MD

From the Cardiovascular Imaging Center, Department of Cardiology, Cleveland Clinic Foundation, Cleveland, Ohio (D.Y.L., I.W.B., R.A.G., W.J.S., J.D.T.); and the Department of Cardiology, Prince Henry Hospital, Sydney, Australia (G.B.C., W.F.W.).

Correspondence to Dr Dominic Y. Leung, Department of Cardiology, Desk F15, The Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH 44195.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose This study examined whether patients suffering from stroke and other systemic embolic events may be selected for transesophageal echocardiography on the basis of clinical and transthoracic echocardiographic findings.

Methods We performed transthoracic and transesophageal echocardiography on 824 patients after stroke and other suspected embolic events. Patients were classified into group A if they were in sinus rhythm and had a normal transthoracic echocardiogram. Group B consisted of all other patients. Transesophageal echocardiographic findings of left atrial spontaneous contrast, left atrial thrombus, complex aortic atheroma, and interatrial septal anomalies were correlated with clinical and transthoracic echocardiographic results.

Results Transesophageal echocardiography detected at least one potential source of embolism in 399 patients (49%): spontaneous contrast in 214 patients (26%), left atrial thrombus in 54 (7%), complex atheroma in 111 (13%), and interatrial septal anomalies in 126 (15%). In group A (n=236), only 3 (1%) had spontaneous contrast, 11 (4.6%) had complex atheroma, and none had left atrial thrombus. In group B (n=588), 211 patients (36%, P<.001) had spontaneous contrast, 54 (9.2%, P<.001) had atrial thrombus, and 100 (17%, P<.001) had complex atheroma. Interatrial septal anomalies were detected in similar proportions of patients (18% in group A versus 14% in group B). Left atrial spontaneous echo contrast, thrombus, and complex atheroma were significantly more prevalent in older patients, but interatrial septal anomalies were more prevalent in younger patients irrespective of transthoracic echocardiographic findings. Multivariate analysis identified both an abnormal transthoracic echocardiogram and patient age to be independent predictors of transesophageal echocardiographic findings of left atrial spontaneous echo contrast, left atrial thrombus, or complex atheroma.

Conclusions Transesophageal echocardiography has a low yield for left atrial spontaneous contrast, left atrial thrombus, or complex aortic atheroma in patients with normal transthoracic echocardiogram and sinus rhythm and in younger patients. Interatrial septal anomalies are more prevalent in younger patients. Transthoracic echocardiogram should be performed in patients after stroke or systemic embolic events as a noninvasive screening tool. We recommend transesophageal echocardiogram for patients with abnormal transthoracic echocardiogram and in younger patients when the finding of a patent foramen ovale may contribute to patient management.

Key Words: cardioembolic stroke • echocardiography • embolism

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Transesophageal echocardiography (TEE) is useful in detecting potential intrathoracic sources of embolism^{1 2 3 4 5 6 7} and is often performed in patients who have suffered from stroke or other systemic embolic events. However, it is still controversial whether all such patients should undergo TEE, and there have been no established guidelines for patient selection.

Transthoracic echocardiography (TTE), though a powerful noninvasive tool for the assessment of cardiac chamber size, function, and valvular disease, is insensitive in detecting intrathoracic sources of embolism.⁸ Left atrial spontaneous echo contrast, left atrial thrombus, and mobile pedunculated aortic atheroma, which are high risk factors for subsequent thromboembolism,^{9 10} are usually not visualized by TTE.^{1 2 3 4 5 6 7} However, the role of TTE in selecting patients after stroke or other embolic events for TEE has not been examined. The purpose of this study was to examine whether these patients can be selected for TEE on the basis of clinical and TTE findings.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The study population comprised 824 consecutive patients referred to the echocardiography laboratories for TEE at The Cleveland Clinic Foundation (Cleveland, Ohio) and Prince Henry Hospital (Sydney, Australia) with a diagnosis of stroke, transient ischemic attack, or systemic peripheral embolism from 1988 through 1993. The diagnoses of these events were made by the referring physicians. Patients from Prince Henry Hospital (n=632) were identified prospectively; clinical data, including demographic data, cardiac rhythm, type of systemic embolic event, and interval between the index event and TEE, were obtained by patient interview and chart review at the time of the echocardiographic studies. The initial 115 patients have been reported in part in previous publications.^{2 9 11} Patients from The Cleveland Clinic Foundation (n=192) were identified retrospectively from a computerized database, and clinical data were obtained by chart review.

All patients underwent both TTE and TEE. Echocardiographic examinations were performed with commercially available systems (Hewlett-Packard Sonos 1000 or 1500, Acuson 128 XP) equipped with 2.5- and 3.5-MHz phased-array transthoracic transducers and 5-MHz transesophageal transducers. Transthoracic studies were performed from all standard echocardiographic windows. Global left ventricular systolic function was assessed semiquantitatively from the parasternal and apical views and graded as normal or mild, moderate, or severe impairment. The mitral and aortic valves were assessed by color, pulsed, and continuous-wave Doppler. Mitral and aortic regurgitation, if present, were graded as trivial, mild, moderate, or severe.^{12 13} Left atrial dimension and left ventricular wall thickness were measured according to standard M-mode criteria.¹⁴ The presence of left ventricular hypertrophy was also assessed semiquantitatively. Patients were classified into two groups on the basis of clinical and TTE findings. Group A consisted of patients with normal TTE and normal sinus rhythm. A TTE was considered normal when all of the following criteria were met: (1) normal left ventricular systolic function with no left ventricular hypertrophy, (2) no prosthetic valve, (3) no valvular stenosis and no more than mild mitral or aortic regurgitation, (4) left atrium dimension of 40 mm, and (5) no visualized valvular vegetation or intracardiac masses. Group B consisted of all other patients. We chose these criteria to focus on the strength of TTE while accepting its low sensitivity for left atrial spontaneous echo contrast, thrombus, and aortic atheroma.

TEE was performed according to standard protocols.¹⁵ All TEE examinations were performed within 48 to 72 hours of the corresponding transthoracic studies. Approximately 13% were monoplane, 43% biplane, and 44% multiplane studies. The presence of the following potential sources of embolism was specifically examined: (1) left atrial spontaneous echo contrast and thrombus; (2) atheroma in the thoracic aorta; (3) patent foramen ovale, atrial septal defect, and atrial septal aneurysm; and (4) others, including valvular vegetations and intracardiac masses. Left atrial spontaneous echo contrast was diagnosed by the presence of characteristic dynamic smokelike swirling echo in the left atrium or the atrial appendage, distinct from background white noise due to excessive gain.¹⁶ Left atrial thrombus was diagnosed by the presence of an echodense mass in the left atrium or the left atrial appendage, distinct from the endocardium and the pectinate muscles of the left atrial appendage.¹⁷ The presence of atheroma in the thoracic aorta was examined. Atheroma that were mobile, pedunculated, or protruding 5 mm into the lumen were classified as complex atheroma.^{18 19} All other sessile atheroma <5 mm in thickness were classified as simple atheroma. The interatrial septum was examined for patent foramen ovale, atrial septal defect, and atrial septal aneurysm. Bubble contrast study with agitated saline was performed in all patients to look for interatrial shunting. Bubbles appearing in the left atrium within three cardiac cycles or observed traversing the interatrial septum constituted a positive study for shunting. Atrial septal aneurysm was defined as a thin-walled area in the region of the fossa ovalis with a base of at least 1.5 cm and an excursion with the cardiac cycle of at least 1.5 cm.²⁰ Care was taken to distinguish a true atrial septal aneurysm from a hypermobile interatrial septum.

Results are expressed as mean±SD where appropriate. The ² test or Fisher's exact test was used to compare categorical variables. A multiple logistic regression model (maximum likelihood method) was used to examine the relative value of TTE and patient age (as a continuous variable) in predicting TEE findings of left atrial spontaneous echo contrast, left atrial thrombus, or complex aortic atheroma. Odds ratios were shown with 95% confidence intervals, and statistical significance was defined as a two-tailed value of P<.05.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
A total of 824 patients were studied. There were 463 men and 361 women with a mean age of 63±15 years. Five hundred eighty-three patients (71%) were in sinus rhythm and 241 (29%) in atrial fibrillation. Five hundred twenty-three patients (64%) had suffered a stroke, 145 (18%) transient ischemic attack, 114 (14%) acute embolism to an extremity, and 42 (4%) had other events, including visceral embolism. Ninety-eight percent of these events had occurred within 1 month of the echocardiographic studies. Twenty-five patients (3%) had an aortic valve prosthesis, another 23 patients (3%) had a mitral prosthesis, and 2 other patients had had mitral valve repair. Results of TTE are presented first, followed by TEE findings.

One hundred forty-five patients (18%) had left ventricular systolic dysfunction, which was mild in 56, moderate in 54, and severe in 35. TTE detected left ventricular apical thrombus in 9 patients (1%). All 9 patients had impaired left ventricular function. Three hundred thirteen patients (38%) had left ventricular hypertrophy, which was considered mild in 245 and severe in 68. Twenty-nine patients had aortic stenosis or more than mild aortic regurgitation, and another 23 had mitral stenosis. Nineteen patients (2%) had moderate and 7 patients (0.8%) had severe mitral regurgitation. TTE detected aortic valve vegetations in 2 patients and mitral valve vegetations in another 3 patients. No other intracardiac masses were detected by TTE. The mean left atrial dimension was 41.5±9 mm, with 401 patients (48%) having a left atrial dimension of >40 mm. TTE was considered normal in 240 patients (29%), of whom 236 were in normal sinus rhythm. Group A comprised the latter 236 patients, whereas the remaining 588 patients (61%) constituted group B.

TEE detected at least one potential source of embolism in 399 patients (49%). Left atrial spontaneous echo contrast was detected in 214 patients (26%). Fifty-four patients (7%) had left atrial thrombus, of which 46 (6%) were in the left atrial appendage, 5 in the left atrial cavity, and 3 involved both the left atrial appendage and cavity. Two hundred fifty-five patients (31%) were found to have simple aortic atheroma, and 111 patients (13%) had complex atheroma in the thoracic aorta. A patent foramen ovale was detected in 110 (13%), atrial septal defect in 8 (1%), and atrial septal aneurysm in another 8 patients (1%). TEE confirmed TTE findings of valvular vegetations in the 5 patients and detected vegetations on an aortic prosthesis in 2 additional patients and vegetation on a mitral prosthesis in another. TEE also visualized strands on a native aortic or mitral valve in another 7 patients. No left atrial myxoma or other intracardiac masses were found in our patients.

Table 1 shows the clinical, TEE, and TTE findings according to the preceding clinical events. Compared with patients who had suffered from either transient ischemic attack or stroke, patients suffering from peripheral embolism were more likely to have left atrial enlargement and complex thoracic atheroma. However, there was no significant difference in other clinical, TEE, and TTE findings among the three types of embolic events.

View this table: [in this window] [in a new window]   Table 1. TABLE 1. Clinical and Transthoracic and Transesophageal Echocardiographic Findings of Patients According to Clinical Events

The Figure shows the results of the TEE in patient groups A and B. Left atrial spontaneous echo contrast was detected in only 3 patients (1%) in group A compared with 211 patients (36%) in group B (P<.001). Two of the 3 patients with left atrial spontaneous echo contrast in group A had a history of paroxysmal atrial fibrillation. All left atrial thrombi were found in patients in group B (P<.001). Complex thoracic aortic atheroma was detected in 11 patients (4.6%) in group A compared with 100 patients (17%) in group B (P<.001). An abnormal TTE according to the above-mentioned criteria identified 95% of all patients with left atrial spontaneous echo contrast or left atrial thrombus or complex atheroma. However, abnormalities of the interatrial septum, including patent foramen ovale, atrial septal defect, or aneurysm, were found in roughly similar proportions of patients in both groups (18% versus 14%, P=NS). No patient in group A aged 50 years or less had left atrial spontaneous echo contrast, left atrial thrombus, or complex aortic atheroma.

View larger version (24K): [in this window] [in a new window]   Figure 1. Bar graph shows transesophageal echocardiographic findings in patient group A (normal transthoracic echocardiogram [TTE] and sinus rhythm) and group B (all others). LA indicates left atrium; PFO, patent foramen ovale; ASD, atrial septal defect; and ASA, atrial septal aneurysm.

Sixty-five patients (8%) with atrial fibrillation were found to have left ventricular systolic dysfunction. Eighteen of these 65 patients (28%) had left atrial thrombus, 52 (80%) had left atrial spontaneous echo contrast, and 16 (25%) had complex aortic atheroma. TEE detected at least one of the above three potential sources of embolism in 57 of the 65 patients (90%).

Table 2 shows the results of the TEE when all study patients were subdivided according to patient age, irrespective of the results of their TTE. Dividing ages of 40, 50, and 60 years were used. The prevalences of left atrial spontaneous echo contrast, left atrial thrombus, and complex aortic atheroma were consistently lower in younger patients compared with older patients, irrespective of the dividing age. In contrast, the prevalence of interatrial septal anomalies was higher in the younger patients, except with a dividing age of 60 years.

View this table: [in this window] [in a new window]   Table 2. TABLE 2. Transesophageal Echocardiographic Findings of Patients Subdivided According to Age Irrespective of Transthoracic Echocardiographic Findings

Multiple logistic regression showed that both an abnormal TTE (odds ratio, 8.9; 95% confidence interval, 6.7 to 12.1; P<.0001) and patient age (odds ratio, 1.05; 95% confidence interval, 1.04 to 1.06; P<.0001) are independent predictors of TEE findings of left atrial spontaneous echo contrast, left atrial thrombus, or complex atheroma.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The present study represents the largest reported series of consecutive patients referred for TEE after stroke or other suspected systemic embolic events. It confirms the utility of TEE in detecting potential intrathoracic sources of embolism in these patients. Left atrial thrombus was detected in 7% of our patients, left atrial spontaneous echo contrast in 26%, and complex thoracic aortic atheroma in 13%. The vast majority of the patients (95%) with these abnormalities had an abnormal TTE. Interatrial septal anomalies, detected in 15% of our patients, were more common in younger patients.

This study systematically examined the value of clinical and TTE findings in selecting patients for TEE after stroke or systemic embolic events. TTE plays a complementary role in the noninvasive detection of left ventricular dysfunction, hypertrophy, valvular disease, and left atrial enlargement and is often performed before TEE in these patients. Various investigators have suggested that the yield of TEE for potential intracardiac sources of embolism tended to be higher in patients with clinically suspected heart disease.^{1 3 6 21} In the present study, 95% of all patients with left atrial spontaneous echo contrast, left atrial thrombus, or complex aortic atheroma had an abnormal TTE and/or atrial fibrillation. Ninety percent of all patients with impaired left ventricular function and in atrial fibrillation were found to have at least one of the above abnormalities by TEE. In contrast, TEE had a very low yield for these abnormalities in patients with normal TTEs. These findings are perhaps not surprising given the strong association between left atrial spontaneous echo contrast, left atrial thrombus, left atrial enlargement, mitral valve disease, and atrial fibrillation.^{9 11 16} Left atrial spontaneous echo contrast has also been shown to be significantly associated with complex aortic atheroma.⁹ Furthermore, the value of a normal TTE in identifying a subgroup of patients with a very low prevalence of the above TEE findings is independent of patient age.

Older patients had a higher prevalence of left atrial spontaneous echo contrast, thrombus, and complex atheroma, irrespective of the dividing age and results of their TTEs. The prevalences of heart disease and atrial fibrillation, and hence the potential sources of embolism, increase with age. These findings are consistent with the results of the Stroke Prevention in Atrial Fibrillation II Study,²² which suggested that older patients had a higher thromboembolic risk reduction with anticoagulation, although at the expense of an increased bleeding risk. The risk-benefit ratio of anticoagulation may be further improved by TEE by allowing selective treatment of those patients with these abnormalities. While our study suggests that the prevalence of interatrial septal anomalies is not significantly affected by the presence of other structural heart diseases, their prevalence is significantly higher in younger patients. Although this finding could represent an age-related decrease in the prevalence of these anomalies,²³ it may also suggest that these anomalies could be related to embolic events and therefore that their detection may be potentially more important in the younger age group.

The decision to perform TEE in patients after stroke or other embolic events should be based on the likelihood of the findings contributing to patient management. The presence of left atrial thrombus increases the risk of subsequent thromboembolism. In the absence of contraindications, warfarin therapy may be considered on their detection. Left atrial spontaneous echo contrast may represent a hypercoagulable state²⁴ and has been shown to be predictive of future thromboembolic events.⁹ Preliminary data suggest that warfarin therapy may be associated with a reduced risk of subsequent thromboembolism.⁹ Complex or protruding aortic atheromas seen on TEE have been shown to predispose to future vascular events¹⁰ and are associated with a higher rate of perioperative stroke in patients undergoing cardiopulmonary bypass.¹⁸ Although warfarin or antiplatelet therapy for complex aortic atheroma is empirical with no proven efficacy, the detection of such atheroma by TEE may still be worthwhile because invasive intravascular procedures can be avoided and aortic cannulation during cardiopulmonary bypass modified.

Paradoxical embolism through a patent foramen ovale, atrial septal defect, and aneurysm is a well-recognized mechanism for systemic thromboembolism, and there have been isolated case reports showing thrombus straddling a patent foramen ovale.^{25 26 27} Although several studies have suggested that interatrial septal anomalies were more prevalent in patients with unexplained stroke than in control subjects,^{28 29} others failed to demonstrate such an association.^{30 31} Moreover, patent foramen ovale is a common finding in the general population. Up to 20% of the control subjects in these studies were found to have a patent foramen ovale,²⁸ and autopsy studies²³ have shown that patent foramen ovale was detected in up to 27% of otherwise normal hearts. The causal relationship between the detection of interatrial septal anomalies and embolism may be difficult to establish in a given patient. Although the clinical significance of these anomalies is still unclear, their detection by TEE may be indicated, especially in patients with recurrent or unexplained events. Moreover, as the results of our study suggest, detection of these anomalies may be more important in younger patients in whom the prevalence of these anomalies is higher and other detectable sources of embolism less frequent.

Our study patients were a selected group who were referred for TEE and were not true consecutive patients admitted with stroke or other systemic embolic events. The true prevalence of the various sources of embolism might have been lower had all such patients been included. We did not have a control group of patients with no history of embolism. However, this is unlikely to affect the validity of our observations, which were made from comparisons of the results of TTE and TEE of our study patients. The reported prevalence of patent foramen ovale ranged from 3% to 47%^{6 21 28 30 31 32 33} and that for atrial septal aneurysm ranged from 1% in autopsy series³⁴ to 3% to 16%^{1 21 35 36} in TEE series, depending on the patient population studied and diagnostic tests and criteria used. Pearson and coworkers¹ reported a 21% prevalence of atrial septal aneurysm in a selected population with no cardiac disease, stroke, or transient ischemic attack. The relatively low 13% prevalence of patent foramen ovale in our study may have been due to the fact that our patients belonged to a more elderly population and that multiple contrast injections were not routinely performed. The low 1% prevalence of atrial septal aneurysm may have been due to our use of strict diagnostic criteria restricting the diagnosis to true aneurysms instead of hypermobile interatrial septum with a wide base. Our classification system of normal TTE is not perfect (sensitivity, 95%); 3 patients with left atrial spontaneous echo contrast and 11 patients with complex aortic atheroma had a normal TTE. Therefore, these diagnostic guidelines should be used in conjunction with clinical judgment in each individual case.

In addition to being a noninvasive screening tool for patients after stroke or systemic embolic events, TTE may assist in the selection of patients for TEE. The results of the present study suggest that the type of embolic source detectable by TEE may reasonably be predicted on the basis of clinical and TTE findings, so that the clinician can decide whether TEE is indicated in a given patient. We recommend TEE in patients with abnormal TTE, especially when the decision to give long-term systemic anticoagulation is being considered. The prevalences of left atrial thrombus, spontaneous echo contrast, and complex aortic atheroma are higher in this subset of patients, and the detection of these abnormalities may help guide further therapy. In patients with normal TTE, the decision to perform TEE should be based on the perceived importance of possible findings of interatrial septal anomalies. TEE may be recommended in younger patients with otherwise unexplained events in whom patent foramen ovale is more prevalent and is potentially of higher importance. However, in older patients in whom the finding of patent foramen ovale may not be as relevant, TEE may contribute little in the process of clinical decision making. Whether the overall cost-effectiveness of TEE in these patients can be improved by this approach needs to be examined by future studies.

	Acknowledgments

 
We would like to thank Annitta Morehead, RDCS, and David Law, BSc, for their assistance in data collection.

Received February 13, 1995; revision received June 26, 1995; accepted June 28, 1995.

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