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The Role of Transesophageal Echocardiography in the Diagnosis and Treatment of Right Atrial Thrombi
The Role of Transesophageal Echocardiography in the Diagnosis and Treatment of Right Atrial Thrombi Arthur Z. Schwartzbard, MD, Paul A. Tunick, MD, Barry P. Rosenzweig, MD, and Itzhak Kronzon, MD, New York, New York
Twenty patients with right atrial thrombi were identified through the use of transthoracic and transesophageal echocardiography. Transesophageal echocardiography identified right atrial thrombi in all 20 cases. Transthoracic echocardiography showed definite thrombi in only 6 (30%) cases and suggested thrombus in another 2 (10%) patients. Thus transthoracic echocardiography results were false-negative for right atrial thrombus in 60% of cases. All 3 thrombi found within the right atrial appendage and 2 of 3 thrombi on pacemaker wires were missed by transthoracic echocardiography. There was no significant difference in the mean size between those thrombi seen (1.37 ± 0.6 cm) and those missed (1.5 ± 0.9 cm) by
R ight atrial thrombi are rare but often clinically significant. They may be seen in association with pulmonary emboli or as unexpected findings on echocardiography.1 Several reports have focused on the role of 2-dimensional transthoracic echocardiography (TTE) in the diagnosis2-6 and management7,8 of right atrial thrombi. Transesophageal echocardiography (TEE) is superior to TTE for the evaluation of patients with intracardiac masses,9-13 and multiple case reports have shown that right atrial thrombi may be seen by TEE.14-19 This study was undertaken to assess the contribution of TEE to the diagnosis and management of a series of patients with right atrial thrombi.
METHODS Databases including 61,253 TTEs and 6254 TEEs performed at New York University Medical Center (Tisch Hospital and
From the Charles and Rose Wohlstetter Noninvasive Cardiology Laboratory, Department of Medicine, New York University Medical Center, New York, NY. Reprint requests: Paul A. Tunick, MD, New York University Medical Center, 560 First Ave, New York, NY 10016. Copyright © 1999 by the American Society of Echocardiography. 0894-7317/99/$8.00 + 0 27/1/93878
64
transthoracic echocardiography. Transesophageal echocardiography also significantly affected treatment. Anticoagulation was initiated or amplified in 13 patients. In 8 of these 13, thrombi were seen only by transesophageal echocardiography. Surgery was performed to remove thrombi in 7 cases, and in 3 (43%) cases it was because of thrombi seen only by transesophageal echocardiography. This study suggests that transesophageal echocardiography should be performed whenever right atrial thrombi are suspected. Transesophageal echocardiography has a significant effect on the diagnosis and management of patients with right atrial thrombi. (J Am Soc Echocardiogr 1999;12:64-9.)
Bellevue Hospital) between 1989 and 1996 were interrogated. All echocardiograms showing right atrial thrombi were included in the study (all patients with TTE evidence of thrombus also had TEE).They were each reviewed by 2 of the authors for the following data: number of thrombi and their size, mobility, location, and extension into the great vessels or other cardiac chambers. Right ventricular wall motion and tricuspid valve function were evaluated, and an estimation of pulmonary artery systolic pressure was made from the velocity of the tricuspid regurgitation jet imaged by continuous wave Doppler. The cardiac rhythm and presence or absence of spontaneous echo contrast (“smoke”) were recorded. Patient medical records were then reviewed and physician follow-up obtained to determine clinical outcomes and whether or not patient treatment had been affected by the results of the TEE. Echocardiography TTE was performed in the routine fashion.The right atrium was visualized from the parasternal short-axis and right ventricular inflow views, the apical 4-chamber view, and the subxiphoid view. For TEE, informed consent was obtained from all patients. TEEs were performed on the same day as the TTE in 15 of 20 patients and within 24 hours of the TTE in all patients. Studies were performed in the noninvasive cardiology laboratories or at the bedside as necessary, after a 4-hour fast.The oropharynx was anes-
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Schwartzbard et al 65
Table 1 Characteristics for patients with right atrial thrombi Patient No.
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
Age
Location
Size/TTE (cm)
Size/TEE (cm)
Mobile
76 34 58 64 54 32 59 73 70 35 29 13 81 76 86 81 38 64 32 24
Body Body Body Body Pacemaker Body Pacemaker Appendage Body Body Body Body Body Body Appendage Appendage Body Body Body Pacemaker
1.1 1.5 0.8 0.5 0.5 1.3 Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen
1.2 2.5 1.0 1.0 1.0 1.5 2.0 2.0 1.0 1.8 2.5 2.0 3.6 1 1 1 1.1 0.7 1.5 0.7
Yes Yes Yes Yes Yes No Yes No No No Yes Yes No Yes No Yes Yes Yes Yes Yes
AF
“Smoke” Extension (TEE) Surgery Death
PA IVC PFO PFO
+ + +
+
SVC
+
+ +
+
+ +
+
+ IVC
+
+ + + + + +
+
+ + +
AF, Atrial fibrillation; IVC, inferior vena cava; PA, pulmonary artery; PFO, patent foramen ovale; SVC, superior vena cava; TEE, transesophageal echocardiogram; TTE, transthoracic echocardiogram.
thetized with topical lidocaine spray. No other premedication was administered. All patients were studied with either a 5-MHz biplane or multiplane transducer.The right atrial appendage was best visualized with a horizontal (0 degree) view.The images were reviewed from videotape. Definition of Right Atrial Thrombus Right atrial thrombus was defined as a right atrial mass meeting 1 or more of the following criteria: serpiginous mobile mass representing a cast of a leg vein; location in the right atrial appendage or on a pacing wire with no clinical evidence to suggest endocarditis; resolution with anticoagulation; or pathologic confirmation at surgery. Masses with characteristic appearance of normal variant structures (Chiari network or prominent Eustachian valve) were excluded. Valvular masses (vegetations or tumors), masses attached by a stalk to the interatrial septum (myxomas), and masses subsequently proven pathologically to be tumors were also excluded.There was complete agreement in identifying right atrial masses between the original clinical interpretation and those of the authors at the time of the study.
RESULTS The results are summarized in Table 1. Patient Characteristics Twenty patients (12 women) ranging in age from 13 to 86 years (mean 54 ± 22) with right atrial thrombi
were identified. Atrial fibrillation was present in 9 (45%) of 20 patients. Spontaneous echo-contrast (“smoke”) was present in the right atrium of 5 (25%) of 20 patients, and 4 (80%) of these 5 evidenced atrial fibrillation. Indications for having performed a TEE in these patients were varied, and included the suspicion of right atrial thrombus on TTE (8 patients), evaluation for an embolic source of ischemic brain events (3 patients), monitoring and guiding transseptal puncture during mitral balloon valvuloplasty (2 patients), dyspnea and/or rule-out pulmonary embolus (3 patients) and assessment of the severity of mitral regurgitation, evaluation after cardiac arrest, evaluation before cardioversion, and tricuspid valve dysfunction (1 patient each). Eight patients were given anticoagulation therapy with warfarin before their echocardiograms.Three patients had pacemaker wires in situ. Diagnosis of Right Atrial Thrombi TEE identified right atrial thrombi in all 20 cases.TTE showed definite thrombi in only 6 (30%) cases and suggested thrombus in another 2 (10%) patients. Thus TTE results were false-negative for right atrial thrombus in 60% of cases. Furthermore, TTE never showed more than 1 thrombus, whereas multiple thrombi were found in 11 (55%) of 20 patients by TEE.All 3 of the thrombi found within the right atrial appendage (Figure 1) were missed by TTE, and TTE also missed 2 of the 3 thrombi found on pacemaker wires.
66 Schwartzbard et al
Journal of the American Society of Echocardiography January 1999
Figure 1 Transesophageal echocardiogram (horizontal plane; 0 degree). Note thrombus in the right atrial appendage (arrows). LA, Left atrium; RA, right atrium.
Five of the 6 thrombi seen on TTE were mobile, and 5 of the 6 nonmobile thrombi were missed by TTE.The patients with nonmobile thrombi were significantly older than those with mobile thrombi (63 ± 23 vs 50 ± 22 years).All TTE studies were judged to be of good or excellent quality.Therefore, the quality of the images obtained from the transthoracic approach was not a factor in the insensitivity of TTE for the diagnosis of right atrial thrombi.
TEE Affects Patient Treatment The visualization of right atrial thrombus frequently led to changes in patient treatment. Anticoagulation therapy was initiated or amplified in 13 patients. In 8 (62%) of these 13 patients, the thrombi were seen only by TEE and were missed by TTE. Surgery was performed to remove thrombi in 7 patients, and in 3 (43%) cases it was because of thrombus seen only by TEE.
Size of Thrombi
Hospital Course
Right atrial thrombi were definitely seen by TTE in only 6 patients. Their sizes as measured by TTE ranged from 0.5 to 1.5 cm (mean 0.95 cm); by TEE, these same thrombi ranged from 1.0 to 2.5 cm (mean 1.37 cm), a 44% difference. Therefore TTE is likely to have underestimated the sizes of these thrombi. In addition, there was no significant difference in the mean size (as measured by TEE) between those thrombi seen on TTE (1.37 ± 0.6 cm) and those missed by TTE (1.5 ± 0.9 cm); hence size did not prove to be a factor in the ability of TTE to visualize right atrial thrombi.
In our series, 7 (35%) of 20 patients underwent surgical removal of thrombi, and none of those operated died. There were 2 deaths in the entire series (mortality rate of 10%), and both occurred in unoperated patients with mobile thrombi. Fourteen patients had mobile thrombi. Five of these were operated on acutely, and all survived. There were 2 deaths in the 9 unoperated patients with mobile thrombi. One patient was in cardiac arrest, and urgent TTE revealed a mobile thrombus only in the right atrium. TEE immediately followed and revealed additional thrombi in the right and left pulmonary arteries.The patient died before any operative intervention. The second patient died suddenly, 2 weeks after the diagnosis of thrombus on a pacing wire. No autopsy was performed. Therefore the mortality rate in this group with mobile thrombi was 14% (2 of 14 patients). There were no deaths in the 6 patients with non-
Thrombi in Other Cardiac Locations Only TEE showed extension of thrombus into the superior vena cava (1 patient), into the inferior vena cava (2 patients), and across a patent foramen ovale into the left atrium (in 1 of 2 patients with this finding) (Figure 2). In addition, only TEE showed thrombi in the pulmonary arteries (1 patient).
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Schwartzbard et al 67
Figure 2 Transesophageal echocardiogram (horizontal plane; 0 degree). Note multilobed thrombus (arrows) in the right atrium, crossing a patent foramen ovale into the left atrium. LA, Left atrium; RA, right atrium.
mobile thrombi.Two were operated on acutely and 4 were treated medically. Additional Information Obtained by Echocardiography Right ventricular systolic function was decreased in 3 (15%) of 20 patients. In 2 (10%) other patients, the right ventricle was dilated but right ventricular systolic function was normal. Concomitant tricuspid valve disease was present in 12 (60%) of 20 cases; 10 of 20 patients (50%) had significant (moderate or severe) tricuspid regurgitation, and 2 patients (10%) had tricuspid prostheses. Pulmonary artery systolic pressure, as estimated from the velocity of the tricuspid regurgitation with the modified Bernoulli equation, was 40 mm Hg or more in 9 (45%) of 20 cases. Spontaneous echo contrast (present in 4 of 5 patients with atrial fibrillation) was seen in the right atrium only by TEE.
DISCUSSION Previous reports have suggested that right atrial thrombi, while rare, may have grave consequences, including pulmonary embolism and death.1,20 Several reports focused on the role of 2-dimensional echocardiography in visualizing right atrial thrombi and on distinguishing them from other right atrial
masses.1-6 The differential diagnosis includes tumors (especially myxomas), normal variants (Chiari network or prominent Eustachian valves), vegetations, artifacts, foreign bodies (pulmonary artery catheters or pacing wires), and aneurysm of the sinus of Valsalva. Echocardiographers have focused on characteristics of the right atrial masses that would allow their identification as thrombi.2-6 The serpiginous nature of migrating thromboemboli is said to be unique, leading to accurate identification by echocardiography.6,21 In contrast, pedunculated masses attached to the interatrial septum suggest the diagnosis of myxoma.1 We have found that TTE is relatively insensitive for the detection of right atrial thrombi. One reason for this in the current study is the location of thrombi in the right atrial appendage, an area not well visualized by TTE. In addition,TTE missed 2 of 3 thrombi associated with pacemaker wires.TTE is also not a good technique for visualizing the superior portion of the body of the right atrium. TEE is superior for the demonstration of the interatrial septum,22,23 thus the extension of 2 thrombi through a patent foramen ovale was demonstrated by TEE in both patients and missed by TTE in one. Such extension is a grave risk for cerebral and peripheral embolization. TEE can better visualize the superior and inferior vena cavae24,25 and identify thrombi in these veins
68 Schwartzbard et al
and in the pulmonary arteries.16,26 In the current series, only TEE demonstrated the extension of thrombus into the cavae and pulmonary artery. Furthermore, others have suggested that the improved image resolution provided by TEE allows for the better assessment of thrombus size, suggesting a potentially useful role in the follow-up of patients when treated with anticoagulants or thrombolytic agents.27 We confirmed this observation because the sizes of thrombi measured on TEE were significantly larger than the sizes of the same thrombi measured by TTE. Therefore, TEE better measures thrombus size, but location and immobility rather than size appear to be the factors that reduce the sensitivity of TTE. In previous reports, 2 types of right atrial thrombi are described.1,7,20 Primary thrombi, which develop within the right atrium, are usually nonmobile and are found in conditions of blood stasis. In contrast, secondary thrombi resulting from venous embolization are usually highly mobile and are seen only when trapped in the right heart.A much worse prognosis has been reported for secondary thrombi, as they are associated with a higher incidence of pulmonary embolism and death.1,20 Kronik20 reported a 44% early (≤8 days) mortality rate in patients with “high risk” thrombi, whereas those with primary (sessile) thrombi had a much lower mortality rate (9%). In our series, 14 patients had mobile thrombi, with 2 deaths. Five of these patients were operated on acutely, and all survived. The 2 deaths in our series occurred in the remaining group of 9 patients with mobile thrombi who did not undergo surgery.The reasons for the lower mortality rate of patients with mobile thrombi in our series (14%) compared with that in the previously reported series20 (44%) are unknown, but prompt anticoagulation and surgery for those patients at highest risk may improve survival. Because our study was not randomized to determine which treatment modality—surgery or anticoagulation—is superior, no definite conclusion regarding the therapy of right atrial thrombi can be reached. No patient was treated with a thrombolytic agent. Farfel et al1 noted that the mortality rate of patients with right atrial thrombi was much higher when patients were not treated surgically (50% mortality rate in the medical group, 15% in the surgical group). Kronik20 also noted that patients with mobile thrombi had a lower mortality rate when treated surgically than when treated with anticoagulation alone (27% vs 54%). In contrast, nonmobile thrombi appear to have a better prognosis than mobile thrombi regardless of which therapy is cho-
Journal of the American Society of Echocardiography January 1999
sen.20 However, because the better outcomes with surgery may be due to selection bias in these retrospective series, the optimal management of this disorder remains to be determined. Limitations One limitation of this study is that except in the operated patients, the diagnosis of right atrial thrombus was not confirmed by pathologic data. However, we believe that the criteria used for the diagnosis were reasonably specific because all 7 operated patients were proved to have thrombi. Because of the irregular and mobile nature of many of the thrombi, their measurement may be less than accurate. However, each echocardiogram was reviewed by 2 of the authors and was carefully evaluated for determination of the maximal thrombus dimension. Furthermore, the comparison of the TEE and TTE sizes is more important than the absolute measurements themselves. One final limitation is that in 5 patients, the TEE was not done on the same day as the TTE. However, in all cases, TEE was performed within 24 hours of the TTE. Conclusions Right atrial thrombi, which were identified on only 20 of the more than 60,000 echocardiograms from our laboratory, are indeed rare.TEE is more sensitive than TTE for the identification of right atrial thrombi. Location, and not size, is the main factor affecting the relative sensitivities of TTE and TEE. In addition, nonmobile thrombi are often missed by TTE.The finding of a right atrial thrombus will often significantly alter therapy. In this series, management of this disorder was changed in 55% of patients because of findings seen only on TEE and missed by TTE. Because the TTE diagnosis of right atrial thrombus was false-negative in 60% of cases,TEE should be performed whenever right atrial thrombi are suspected. TEE will better define the size, the shape, and the site of attachment and will find additional thrombi. Thus TEE should even be performed to evaluate a positive TTE.TEE is superior for the diagnosis and evaluation of right atrial thrombi. REFERENCES 1. Farfel Z, Shecter M, Vered Z, et al. Review of echocardiographically diagnosed right heart entrapment of pulmonary emboli-in-transit with emphasis on management. Am Heart J 1987;113:171-8. 2. Rosenzweig MS, Nanda NC. Two-dimensional echocardiographic detection of circulatory right atrial thrombi. Am Heart J 1982;103:435-6.
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3. Oldershaw PJ. Echocardiographic appearances of right atrial thrombus. Clin Cardiol 1982;5:544-6. 4. Come PC. Transient right atrial thrombus during acute myocardial infarction: diagnosis by echocardiography. Am J Cardiol 1983;51:1228-9. 5. Redish GA, Anderson AL. Echocardiographic diagnosis of right atrial thromboembolism. J Am Coll Cardiol 1983;1: 1167-9. 6. Armstrong WF, Feigenbaum H, Dillon JC. Echocardiographic detection of right atrial thromboembolism. Chest 1985;87:801-6. 7. Felner JM, Churchwell AL, Murphy DA. Right atrial thromboemboli: clinical, echocardiographic and pathophysiologic manifestations. J Am Coll Cardiol 1984;4:1041-51. 8. Cameron J, Pohlner PG, Stafford EG, et al. Right heart thrombus: recognition, diagnosis and management. J Am Coll Cardiol 1985;5:1239-43. 9. Mugge A, Daniel WG, Haverich A, et al. Diagnosis of noninfective cardiac mass lesions by 2-dimensional echocardiography: comparison of the transthoracic and transesophageal approaches. Circulation 1991;83:70-8. 10. Cohen GI, Klein AL, Chan KL, et al. Transesophageal echocardiographic diagnosis of right-sided cardiac masses in patients with central lines. Am J Cardiol 1992;70:9259. 11. Obeid AI, Mudamgha AA, Smulyan H. Diagnosis of right atrial mass lesions by transesophageal and transthoracic echocardiography. Chest 1993;103:1447-51. 12. Leibowitz G, Keller NM, Daniel WG, et al. Transesophageal versus transthoracic echocardiography in the evaluation of right atrial tumors. Am Heart J 1995;130:1224-7. 13. Herrera CJ, Mehlman DJ, Hartz RS, et al. Comparison of transesophageal and transthoracic echocardiography for diagnosis of right-sided cardiac lesions. Am J Cardiol 1992;70: 964-6. 14. Day SM, Rosenzweig BR, Kronzon I. Transesophageal echocardiographic diagnosis of right atrial thrombi associated with the antiphospholipid syndrome. J Am Soc Echocardiogr 1995;8:937-40. 15. Huner JJ, Johnson KR, Karagianes TG, et al. Detection of
Schwartzbard et al 69
16.
17.
18.
19.
20.
21.
22.
23. 24.
25.
26.
27.
massive pulmonary embolus-in-transit by transesophageal echocardiography. Chest 1991;100:1210-14. Willens HJ, Ciralso R, Vuoto T, et al. Combined pulmonary embolectomy and right atrial thrombolectomy guided by transesophageal echocardiography. Am Heart J 1995;130: 180-2. Olson JD, Goldenberg IF, Pedersen W, et al. Exclusion of atrial thrombus by transesophageal echocardiography. J Am Soc Echocardiogr 1992;5:52-6. Pasierski TJ, Alton ME, Van Fossen DB, et al. Right atrial mobile thrombus: improved visualization by transesophageal echocardiography. Am Heart J 1992;123:802-3. Konecky N, Rosenzweig BP, Katz ES, et al. Right atrial thrombus complicating mitral valvuloplasty. Am Heart J 1996;132:893-4. Kronik G. European working group on echocardiography. The European cooperative study on the clinical significance of right heart thrombi. Eur Heart J 1989;10:1046-59. Panidis IP, Kotler MN, Mintz GS, et al. Clinical and echocardiographic features of right atrial masses. Am Heart J 1984; 107:745-58. Barbour SI, Izban KF, Reyes CV, et al. Serpentine thrombus traversing the foramen ovale: paradoxical embolism shown by transesophageal echocardiography. Ann Intern Med 1996: 125:111-3. Rosenzweig BP, Glassman L, Kronzon I. Impending paradoxical embolus. Circulation 1996;93:387. Alam M, Sun I, Smith S. Transesophageal echocardiographic evaluation of right atrial mass lesions. J Am Soc Echocardiogr 1991;4:331-7. Holman WL, Coghlan CH, Dodson MR, et al. Removal of massive right atrial thrombus guided by transesophageal echocardiography. Ann Thorac Surg 1991;52:313-5. Rittoo D, Sutherland GR, Samuel L, et al. Role of transesophageal echocardiography in the diagnosis and management of central pulmonary artery thromboembolism. Am J Cardiol 1993;71:1115-8. Crowley JJ, Kenny A, Dardas P, et al. Identification of right atrial thrombi using transesophageal echocardiography. Eur Heart J 1995;16:708-10.
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Twenty patients with right atrial thrombi were identified through the use of transthoracic and transesophageal echocardiography. Transesophageal echocardiography identified right atrial thrombi in all 20 cases. Transthoracic echocardiography showed definite thrombi in only 6 (30%) cases and suggested thrombus in another 2 (10%) patients. Thus transthoracic echocardiography results were false-negative for right atrial thrombus in 60% of cases. All 3 thrombi found within the right atrial appendage and 2 of 3 thrombi on pacemaker wires were missed by transthoracic echocardiography. There was no significant difference in the mean size between those thrombi seen (1.37 ± 0.6 cm) and those missed (1.5 ± 0.9 cm) by
R ight atrial thrombi are rare but often clinically significant. They may be seen in association with pulmonary emboli or as unexpected findings on echocardiography.1 Several reports have focused on the role of 2-dimensional transthoracic echocardiography (TTE) in the diagnosis2-6 and management7,8 of right atrial thrombi. Transesophageal echocardiography (TEE) is superior to TTE for the evaluation of patients with intracardiac masses,9-13 and multiple case reports have shown that right atrial thrombi may be seen by TEE.14-19 This study was undertaken to assess the contribution of TEE to the diagnosis and management of a series of patients with right atrial thrombi.
METHODS Databases including 61,253 TTEs and 6254 TEEs performed at New York University Medical Center (Tisch Hospital and
From the Charles and Rose Wohlstetter Noninvasive Cardiology Laboratory, Department of Medicine, New York University Medical Center, New York, NY. Reprint requests: Paul A. Tunick, MD, New York University Medical Center, 560 First Ave, New York, NY 10016. Copyright © 1999 by the American Society of Echocardiography. 0894-7317/99/$8.00 + 0 27/1/93878
64
transthoracic echocardiography. Transesophageal echocardiography also significantly affected treatment. Anticoagulation was initiated or amplified in 13 patients. In 8 of these 13, thrombi were seen only by transesophageal echocardiography. Surgery was performed to remove thrombi in 7 cases, and in 3 (43%) cases it was because of thrombi seen only by transesophageal echocardiography. This study suggests that transesophageal echocardiography should be performed whenever right atrial thrombi are suspected. Transesophageal echocardiography has a significant effect on the diagnosis and management of patients with right atrial thrombi. (J Am Soc Echocardiogr 1999;12:64-9.)
Bellevue Hospital) between 1989 and 1996 were interrogated. All echocardiograms showing right atrial thrombi were included in the study (all patients with TTE evidence of thrombus also had TEE).They were each reviewed by 2 of the authors for the following data: number of thrombi and their size, mobility, location, and extension into the great vessels or other cardiac chambers. Right ventricular wall motion and tricuspid valve function were evaluated, and an estimation of pulmonary artery systolic pressure was made from the velocity of the tricuspid regurgitation jet imaged by continuous wave Doppler. The cardiac rhythm and presence or absence of spontaneous echo contrast (“smoke”) were recorded. Patient medical records were then reviewed and physician follow-up obtained to determine clinical outcomes and whether or not patient treatment had been affected by the results of the TEE. Echocardiography TTE was performed in the routine fashion.The right atrium was visualized from the parasternal short-axis and right ventricular inflow views, the apical 4-chamber view, and the subxiphoid view. For TEE, informed consent was obtained from all patients. TEEs were performed on the same day as the TTE in 15 of 20 patients and within 24 hours of the TTE in all patients. Studies were performed in the noninvasive cardiology laboratories or at the bedside as necessary, after a 4-hour fast.The oropharynx was anes-
Journal of the American Society of Echocardiography Volume 12 Number 1
Schwartzbard et al 65
Table 1 Characteristics for patients with right atrial thrombi Patient No.
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
Age
Location
Size/TTE (cm)
Size/TEE (cm)
Mobile
76 34 58 64 54 32 59 73 70 35 29 13 81 76 86 81 38 64 32 24
Body Body Body Body Pacemaker Body Pacemaker Appendage Body Body Body Body Body Body Appendage Appendage Body Body Body Pacemaker
1.1 1.5 0.8 0.5 0.5 1.3 Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen Not seen
1.2 2.5 1.0 1.0 1.0 1.5 2.0 2.0 1.0 1.8 2.5 2.0 3.6 1 1 1 1.1 0.7 1.5 0.7
Yes Yes Yes Yes Yes No Yes No No No Yes Yes No Yes No Yes Yes Yes Yes Yes
AF
“Smoke” Extension (TEE) Surgery Death
PA IVC PFO PFO
+ + +
+
SVC
+
+ +
+
+ +
+
+ IVC
+
+ + + + + +
+
+ + +
AF, Atrial fibrillation; IVC, inferior vena cava; PA, pulmonary artery; PFO, patent foramen ovale; SVC, superior vena cava; TEE, transesophageal echocardiogram; TTE, transthoracic echocardiogram.
thetized with topical lidocaine spray. No other premedication was administered. All patients were studied with either a 5-MHz biplane or multiplane transducer.The right atrial appendage was best visualized with a horizontal (0 degree) view.The images were reviewed from videotape. Definition of Right Atrial Thrombus Right atrial thrombus was defined as a right atrial mass meeting 1 or more of the following criteria: serpiginous mobile mass representing a cast of a leg vein; location in the right atrial appendage or on a pacing wire with no clinical evidence to suggest endocarditis; resolution with anticoagulation; or pathologic confirmation at surgery. Masses with characteristic appearance of normal variant structures (Chiari network or prominent Eustachian valve) were excluded. Valvular masses (vegetations or tumors), masses attached by a stalk to the interatrial septum (myxomas), and masses subsequently proven pathologically to be tumors were also excluded.There was complete agreement in identifying right atrial masses between the original clinical interpretation and those of the authors at the time of the study.
RESULTS The results are summarized in Table 1. Patient Characteristics Twenty patients (12 women) ranging in age from 13 to 86 years (mean 54 ± 22) with right atrial thrombi
were identified. Atrial fibrillation was present in 9 (45%) of 20 patients. Spontaneous echo-contrast (“smoke”) was present in the right atrium of 5 (25%) of 20 patients, and 4 (80%) of these 5 evidenced atrial fibrillation. Indications for having performed a TEE in these patients were varied, and included the suspicion of right atrial thrombus on TTE (8 patients), evaluation for an embolic source of ischemic brain events (3 patients), monitoring and guiding transseptal puncture during mitral balloon valvuloplasty (2 patients), dyspnea and/or rule-out pulmonary embolus (3 patients) and assessment of the severity of mitral regurgitation, evaluation after cardiac arrest, evaluation before cardioversion, and tricuspid valve dysfunction (1 patient each). Eight patients were given anticoagulation therapy with warfarin before their echocardiograms.Three patients had pacemaker wires in situ. Diagnosis of Right Atrial Thrombi TEE identified right atrial thrombi in all 20 cases.TTE showed definite thrombi in only 6 (30%) cases and suggested thrombus in another 2 (10%) patients. Thus TTE results were false-negative for right atrial thrombus in 60% of cases. Furthermore, TTE never showed more than 1 thrombus, whereas multiple thrombi were found in 11 (55%) of 20 patients by TEE.All 3 of the thrombi found within the right atrial appendage (Figure 1) were missed by TTE, and TTE also missed 2 of the 3 thrombi found on pacemaker wires.
66 Schwartzbard et al
Journal of the American Society of Echocardiography January 1999
Figure 1 Transesophageal echocardiogram (horizontal plane; 0 degree). Note thrombus in the right atrial appendage (arrows). LA, Left atrium; RA, right atrium.
Five of the 6 thrombi seen on TTE were mobile, and 5 of the 6 nonmobile thrombi were missed by TTE.The patients with nonmobile thrombi were significantly older than those with mobile thrombi (63 ± 23 vs 50 ± 22 years).All TTE studies were judged to be of good or excellent quality.Therefore, the quality of the images obtained from the transthoracic approach was not a factor in the insensitivity of TTE for the diagnosis of right atrial thrombi.
TEE Affects Patient Treatment The visualization of right atrial thrombus frequently led to changes in patient treatment. Anticoagulation therapy was initiated or amplified in 13 patients. In 8 (62%) of these 13 patients, the thrombi were seen only by TEE and were missed by TTE. Surgery was performed to remove thrombi in 7 patients, and in 3 (43%) cases it was because of thrombus seen only by TEE.
Size of Thrombi
Hospital Course
Right atrial thrombi were definitely seen by TTE in only 6 patients. Their sizes as measured by TTE ranged from 0.5 to 1.5 cm (mean 0.95 cm); by TEE, these same thrombi ranged from 1.0 to 2.5 cm (mean 1.37 cm), a 44% difference. Therefore TTE is likely to have underestimated the sizes of these thrombi. In addition, there was no significant difference in the mean size (as measured by TEE) between those thrombi seen on TTE (1.37 ± 0.6 cm) and those missed by TTE (1.5 ± 0.9 cm); hence size did not prove to be a factor in the ability of TTE to visualize right atrial thrombi.
In our series, 7 (35%) of 20 patients underwent surgical removal of thrombi, and none of those operated died. There were 2 deaths in the entire series (mortality rate of 10%), and both occurred in unoperated patients with mobile thrombi. Fourteen patients had mobile thrombi. Five of these were operated on acutely, and all survived. There were 2 deaths in the 9 unoperated patients with mobile thrombi. One patient was in cardiac arrest, and urgent TTE revealed a mobile thrombus only in the right atrium. TEE immediately followed and revealed additional thrombi in the right and left pulmonary arteries.The patient died before any operative intervention. The second patient died suddenly, 2 weeks after the diagnosis of thrombus on a pacing wire. No autopsy was performed. Therefore the mortality rate in this group with mobile thrombi was 14% (2 of 14 patients). There were no deaths in the 6 patients with non-
Thrombi in Other Cardiac Locations Only TEE showed extension of thrombus into the superior vena cava (1 patient), into the inferior vena cava (2 patients), and across a patent foramen ovale into the left atrium (in 1 of 2 patients with this finding) (Figure 2). In addition, only TEE showed thrombi in the pulmonary arteries (1 patient).
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Schwartzbard et al 67
Figure 2 Transesophageal echocardiogram (horizontal plane; 0 degree). Note multilobed thrombus (arrows) in the right atrium, crossing a patent foramen ovale into the left atrium. LA, Left atrium; RA, right atrium.
mobile thrombi.Two were operated on acutely and 4 were treated medically. Additional Information Obtained by Echocardiography Right ventricular systolic function was decreased in 3 (15%) of 20 patients. In 2 (10%) other patients, the right ventricle was dilated but right ventricular systolic function was normal. Concomitant tricuspid valve disease was present in 12 (60%) of 20 cases; 10 of 20 patients (50%) had significant (moderate or severe) tricuspid regurgitation, and 2 patients (10%) had tricuspid prostheses. Pulmonary artery systolic pressure, as estimated from the velocity of the tricuspid regurgitation with the modified Bernoulli equation, was 40 mm Hg or more in 9 (45%) of 20 cases. Spontaneous echo contrast (present in 4 of 5 patients with atrial fibrillation) was seen in the right atrium only by TEE.
DISCUSSION Previous reports have suggested that right atrial thrombi, while rare, may have grave consequences, including pulmonary embolism and death.1,20 Several reports focused on the role of 2-dimensional echocardiography in visualizing right atrial thrombi and on distinguishing them from other right atrial
masses.1-6 The differential diagnosis includes tumors (especially myxomas), normal variants (Chiari network or prominent Eustachian valves), vegetations, artifacts, foreign bodies (pulmonary artery catheters or pacing wires), and aneurysm of the sinus of Valsalva. Echocardiographers have focused on characteristics of the right atrial masses that would allow their identification as thrombi.2-6 The serpiginous nature of migrating thromboemboli is said to be unique, leading to accurate identification by echocardiography.6,21 In contrast, pedunculated masses attached to the interatrial septum suggest the diagnosis of myxoma.1 We have found that TTE is relatively insensitive for the detection of right atrial thrombi. One reason for this in the current study is the location of thrombi in the right atrial appendage, an area not well visualized by TTE. In addition,TTE missed 2 of 3 thrombi associated with pacemaker wires.TTE is also not a good technique for visualizing the superior portion of the body of the right atrium. TEE is superior for the demonstration of the interatrial septum,22,23 thus the extension of 2 thrombi through a patent foramen ovale was demonstrated by TEE in both patients and missed by TTE in one. Such extension is a grave risk for cerebral and peripheral embolization. TEE can better visualize the superior and inferior vena cavae24,25 and identify thrombi in these veins
68 Schwartzbard et al
and in the pulmonary arteries.16,26 In the current series, only TEE demonstrated the extension of thrombus into the cavae and pulmonary artery. Furthermore, others have suggested that the improved image resolution provided by TEE allows for the better assessment of thrombus size, suggesting a potentially useful role in the follow-up of patients when treated with anticoagulants or thrombolytic agents.27 We confirmed this observation because the sizes of thrombi measured on TEE were significantly larger than the sizes of the same thrombi measured by TTE. Therefore, TEE better measures thrombus size, but location and immobility rather than size appear to be the factors that reduce the sensitivity of TTE. In previous reports, 2 types of right atrial thrombi are described.1,7,20 Primary thrombi, which develop within the right atrium, are usually nonmobile and are found in conditions of blood stasis. In contrast, secondary thrombi resulting from venous embolization are usually highly mobile and are seen only when trapped in the right heart.A much worse prognosis has been reported for secondary thrombi, as they are associated with a higher incidence of pulmonary embolism and death.1,20 Kronik20 reported a 44% early (≤8 days) mortality rate in patients with “high risk” thrombi, whereas those with primary (sessile) thrombi had a much lower mortality rate (9%). In our series, 14 patients had mobile thrombi, with 2 deaths. Five of these patients were operated on acutely, and all survived. The 2 deaths in our series occurred in the remaining group of 9 patients with mobile thrombi who did not undergo surgery.The reasons for the lower mortality rate of patients with mobile thrombi in our series (14%) compared with that in the previously reported series20 (44%) are unknown, but prompt anticoagulation and surgery for those patients at highest risk may improve survival. Because our study was not randomized to determine which treatment modality—surgery or anticoagulation—is superior, no definite conclusion regarding the therapy of right atrial thrombi can be reached. No patient was treated with a thrombolytic agent. Farfel et al1 noted that the mortality rate of patients with right atrial thrombi was much higher when patients were not treated surgically (50% mortality rate in the medical group, 15% in the surgical group). Kronik20 also noted that patients with mobile thrombi had a lower mortality rate when treated surgically than when treated with anticoagulation alone (27% vs 54%). In contrast, nonmobile thrombi appear to have a better prognosis than mobile thrombi regardless of which therapy is cho-
Journal of the American Society of Echocardiography January 1999
sen.20 However, because the better outcomes with surgery may be due to selection bias in these retrospective series, the optimal management of this disorder remains to be determined. Limitations One limitation of this study is that except in the operated patients, the diagnosis of right atrial thrombus was not confirmed by pathologic data. However, we believe that the criteria used for the diagnosis were reasonably specific because all 7 operated patients were proved to have thrombi. Because of the irregular and mobile nature of many of the thrombi, their measurement may be less than accurate. However, each echocardiogram was reviewed by 2 of the authors and was carefully evaluated for determination of the maximal thrombus dimension. Furthermore, the comparison of the TEE and TTE sizes is more important than the absolute measurements themselves. One final limitation is that in 5 patients, the TEE was not done on the same day as the TTE. However, in all cases, TEE was performed within 24 hours of the TTE. Conclusions Right atrial thrombi, which were identified on only 20 of the more than 60,000 echocardiograms from our laboratory, are indeed rare.TEE is more sensitive than TTE for the identification of right atrial thrombi. Location, and not size, is the main factor affecting the relative sensitivities of TTE and TEE. In addition, nonmobile thrombi are often missed by TTE.The finding of a right atrial thrombus will often significantly alter therapy. In this series, management of this disorder was changed in 55% of patients because of findings seen only on TEE and missed by TTE. Because the TTE diagnosis of right atrial thrombus was false-negative in 60% of cases,TEE should be performed whenever right atrial thrombi are suspected. TEE will better define the size, the shape, and the site of attachment and will find additional thrombi. Thus TEE should even be performed to evaluate a positive TTE.TEE is superior for the diagnosis and evaluation of right atrial thrombi. REFERENCES 1. Farfel Z, Shecter M, Vered Z, et al. Review of echocardiographically diagnosed right heart entrapment of pulmonary emboli-in-transit with emphasis on management. Am Heart J 1987;113:171-8. 2. Rosenzweig MS, Nanda NC. Two-dimensional echocardiographic detection of circulatory right atrial thrombi. Am Heart J 1982;103:435-6.
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3. Oldershaw PJ. Echocardiographic appearances of right atrial thrombus. Clin Cardiol 1982;5:544-6. 4. Come PC. Transient right atrial thrombus during acute myocardial infarction: diagnosis by echocardiography. Am J Cardiol 1983;51:1228-9. 5. Redish GA, Anderson AL. Echocardiographic diagnosis of right atrial thromboembolism. J Am Coll Cardiol 1983;1: 1167-9. 6. Armstrong WF, Feigenbaum H, Dillon JC. Echocardiographic detection of right atrial thromboembolism. Chest 1985;87:801-6. 7. Felner JM, Churchwell AL, Murphy DA. Right atrial thromboemboli: clinical, echocardiographic and pathophysiologic manifestations. J Am Coll Cardiol 1984;4:1041-51. 8. Cameron J, Pohlner PG, Stafford EG, et al. Right heart thrombus: recognition, diagnosis and management. J Am Coll Cardiol 1985;5:1239-43. 9. Mugge A, Daniel WG, Haverich A, et al. Diagnosis of noninfective cardiac mass lesions by 2-dimensional echocardiography: comparison of the transthoracic and transesophageal approaches. Circulation 1991;83:70-8. 10. Cohen GI, Klein AL, Chan KL, et al. Transesophageal echocardiographic diagnosis of right-sided cardiac masses in patients with central lines. Am J Cardiol 1992;70:9259. 11. Obeid AI, Mudamgha AA, Smulyan H. Diagnosis of right atrial mass lesions by transesophageal and transthoracic echocardiography. Chest 1993;103:1447-51. 12. Leibowitz G, Keller NM, Daniel WG, et al. Transesophageal versus transthoracic echocardiography in the evaluation of right atrial tumors. Am Heart J 1995;130:1224-7. 13. Herrera CJ, Mehlman DJ, Hartz RS, et al. Comparison of transesophageal and transthoracic echocardiography for diagnosis of right-sided cardiac lesions. Am J Cardiol 1992;70: 964-6. 14. Day SM, Rosenzweig BR, Kronzon I. Transesophageal echocardiographic diagnosis of right atrial thrombi associated with the antiphospholipid syndrome. J Am Soc Echocardiogr 1995;8:937-40. 15. Huner JJ, Johnson KR, Karagianes TG, et al. Detection of
Schwartzbard et al 69
16.
17.
18.
19.
20.
21.
22.
23. 24.
25.
26.
27.
massive pulmonary embolus-in-transit by transesophageal echocardiography. Chest 1991;100:1210-14. Willens HJ, Ciralso R, Vuoto T, et al. Combined pulmonary embolectomy and right atrial thrombolectomy guided by transesophageal echocardiography. Am Heart J 1995;130: 180-2. Olson JD, Goldenberg IF, Pedersen W, et al. Exclusion of atrial thrombus by transesophageal echocardiography. J Am Soc Echocardiogr 1992;5:52-6. Pasierski TJ, Alton ME, Van Fossen DB, et al. Right atrial mobile thrombus: improved visualization by transesophageal echocardiography. Am Heart J 1992;123:802-3. Konecky N, Rosenzweig BP, Katz ES, et al. Right atrial thrombus complicating mitral valvuloplasty. Am Heart J 1996;132:893-4. Kronik G. European working group on echocardiography. The European cooperative study on the clinical significance of right heart thrombi. Eur Heart J 1989;10:1046-59. Panidis IP, Kotler MN, Mintz GS, et al. Clinical and echocardiographic features of right atrial masses. Am Heart J 1984; 107:745-58. Barbour SI, Izban KF, Reyes CV, et al. Serpentine thrombus traversing the foramen ovale: paradoxical embolism shown by transesophageal echocardiography. Ann Intern Med 1996: 125:111-3. Rosenzweig BP, Glassman L, Kronzon I. Impending paradoxical embolus. Circulation 1996;93:387. Alam M, Sun I, Smith S. Transesophageal echocardiographic evaluation of right atrial mass lesions. J Am Soc Echocardiogr 1991;4:331-7. Holman WL, Coghlan CH, Dodson MR, et al. Removal of massive right atrial thrombus guided by transesophageal echocardiography. Ann Thorac Surg 1991;52:313-5. Rittoo D, Sutherland GR, Samuel L, et al. Role of transesophageal echocardiography in the diagnosis and management of central pulmonary artery thromboembolism. Am J Cardiol 1993;71:1115-8. Crowley JJ, Kenny A, Dardas P, et al. Identification of right atrial thrombi using transesophageal echocardiography. Eur Heart J 1995;16:708-10.
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