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Original Article

Improvement in the Diagnosis of Abscesses Associated with Endocarditis by Transesophageal Echocardiography

Werner G. Daniel, M.D., Andreas Mügge, M.D., Randolph P. Martin, M.D., Oliver Lindert, M.D., Dirk Hausmann, M.D., Barbara Nonnast-Daniel, M.D., Joachim Laas, M.D., and Paul R. Lichtlen, M.D.

N Engl J Med 1991; 324:795-800March 21, 1991

Abstract
Abstract

Background.

Echocardiography is recognized as the method of choice for the noninvasive detection of valvular vegetations in patients with infective endocarditis, with transesophageal echocardiography being more accurate than transthoracic echocardiography. The diagnosis of associated abscesses by transthoracic echocardiography is difficult or even impossible in many cases, however, and it is not known whether transesophageal echocardiography is any better.

Methods.

To determine the value of transesophageal echocardiography in the detection of abscesses associated with endocarditis, we studied prospectively by two-dimensional transthoracic and transesophageal echocardiography 118 consecutive patients with infective endocarditis of 137 native or prosthetic valves that was documented during surgery or at autopsy.

Results.

During surgery or at autopsy, 44 patients (37.3 percent) had a total of 46 definite regions of abscess. Abscesses were more frequent in aortic-valve endocarditis than in infections of other valves, and the infecting organism was more often staphylococcus (52.3 percent of cases) in patients with abscesses than in those without abscesses (16.2 percent). The hospital mortality rate was 22.7 percent in patients with abscesses, as compared with 13.5 percent in patients without abscesses. Whereas transthoracic echocardiography identified only 13 of the 46 areas of abscess, the transesophageal approach allowed the detection of 40 regions (P<0.001). Sensitivity and specificity for the detection of abscesses associated with endocarditis were 28.3 and 98.6 percent, respectively, for transthoracic echocardiography and 87.0 and 94.6 percent for transesophageal echocardiography; positive and negative predictive values were 92.9 and 68.9 percent, respectively, for the transthoracic approach and 90.9 and 92.1 percent for the transesophageal approach. Variation between observers was 3.4 percent for transthoracic and 4.2 percent for transesophageal echocardiography.

Conclusions.

The data indicate that transesophageal echocardiography leads to a significant improvement in the diagnosis of abscesses associated with endocarditis. The technique facilitates the identification of patients with endocarditis who have an increased risk of death and permits earlier treatment. (N Engl J Med 1991; 324:795–800.)

Media in This Article

Figure 1Transesophageal Echocardiogram of a Patient with Aortic-Valve Endocarditis.
Figure 2Transesophageal Echocardiogram of a Patient with Endocarditis in a Prosthetic Valve in the Aortic Position.
Article

DURING the past 15 years, echocardiography has become widely accepted as the method of choice for the noninvasive assessment of valvular vegetations in patients with infective endocarditis.1 2 3 4 Reports, however, on the echocardiographic detection of perivalvular abscesses associated with endocarditis are few and incomplete.5 6 7 8 9 10 11 12 13 14 15 16 17 18 On the other hand, abscesses complicating infective endocarditis have been found in up to 30 percent of cases during surgery or at autopsy, and their presence is usually associated with a more severe course of the disease.19 20 21

Recent studies have shown that transesophageal echocardiography, as compared with conventional transthoracic echocardiography, has increased diagnostic accuracy in the detection of valvular vegetations.4 , 22 23 24 We therefore undertook a prospective investigation to assess the value of the transesophageal approach in the detection of abscesses associated with endocarditis.

Methods

Patients

Patients who met the following criteria were included in this study: the presence of acute infective endocarditis, as documented by direct macroscopic inspection and histologic examination during surgery or at autopsy, with or without a perivalvular abscess; and both two-dimensional transthoracic and transesophageal echocardiography performed within seven days before surgery or death. Between January 1984 and May 1989, 118 consecutive patients meeting these criteria were studied prospectively at Hannover Medical School (Hannover, Germany). There were 80 men and 38 women, ranging in age from 17 to 74 years (mean [±SD], 47.8± 14.4). The presence of endocarditis was documented by surgery in 109 patients and by autopsy in 9; 11 of the surgical patients also underwent postoperative autopsy. A total of 137 valves were infected by endocarditis: 59 aortic valves, 41 mitral valves, 3 tricuspid valves, and 34 prosthetic devices (18 mechanical devices and 16 bioprostheses, 19 in the aortic and 15 in the mitral position). During the same period, 28 other patients with infective endocarditis and both transthoracic and transesophageal echocardiographic examinations survived with medical therapy alone; they were excluded from the study since no surgical or autopsy confirmation was available. None of the 28 had an abscess on echocardiography. Two additional patients with severe aortic regurgitation and shock due to endocarditis underwent surgery without transesophageal echocardiography and were also excluded from the present series; in both cases, transthoracic echocardiography and surgery had not revealed an abscess. In all 109 patients in this study who underwent surgery, the indication for the procedure was based on clinical criteria (advanced heart failure or persistent signs of infection); no patient underwent surgery because of an echocardiographically detected abscess alone.

Echocardiography

Transthoracic M-mode and two-dimensional echocardiographic studies were performed by standard techniques with a 2.25- or 3.5-MHz phased-array transducer. For transesophageal echocardiography a 3.5-MHz phased-array transducer. (Diasonic Echoscope, Diasonics Cardio/Imaging, Salt Lake City) or a 5.0-MHz phased-array transducer (model 21362 A, Hewlett—Packard Medical Products Group, Andover, Mass., or Acuson 128 Cardiovascular System, Acuson Computed Sonography, Mountain View, Calif.) was used, the transducer being mounted at the tip of a modified gastroscope. Patients had fasted for at least four hours before echocardiography and received local pharyngeal anesthesia ( 1 percent lidocaine spray) as the only premedication. The investigations were carried out with the patient in the supine left lateral position, as previously described, without any complications.24 , 25 The transesophageal study was usually completed within five minutes. Informed consent was obtained from all the patients.

Definition of Abscess

During surgery or at autopsy (by direct inspection and histopathological examination), an abscess was defined as a region of necrosis containing purulent material and penetrating into the valvular annulus or myocardium.11 , 16 , 26 , 27 An abscess was considered to be present when a definite region of reduced echo density was found on the echocardiograms, or echolucent cavities within the valvular annulas or adjacent myocardial structures were found in the setting of valvular infection. All echocardiograms were evaluated by two independent physicians: the operator of the transesophageal examination evaluated the transthoracic and transesophageal studies immediately after the procedure, and a second physician evaluated the videotape recordings before surgery or autopsy without knowledge of the first evaluation. In cases of disagreement, the observers reevaluated the studies together and a consensus was reached.

Statistical Analysis

For statistical analysis, the chi-square test with Yates' correction for small numbers was used. A P value of less than 0.05 was considered to indicate significance. The sensitivity, specificity, and positive and negative predictive values were calculated for the identification of abscesses by echocardiography.

Results

Anatomical Findings

The anatomical evaluation during surgery or at autopsy revealed a total of 46 definite regions of abscess in 44 of the 118 patients (37.3 percent) (Table 1Table 1Detection of Abscesses Associated with Endocarditis during Surgery or at Autopsy and by Transthoracic and Transesophageal Echocardiography in 118 Patients.*). Fourteen abscesses were found in the aortic root in patients with endocarditis in a native aortic valve, 16 abscesses were located at the ring of an infected aortic prosthetic valve (12 patients, in 2 of whom endocarditis due to Staphylococcus aureus infection in a native valve had developed three and five weeks, respectively, after surgery) or mitral prosthetic valve (4 patients); 9 patients had an abscess of the interventricular septum; in 6 patients with endocarditis in a native mitral valve, abscesses were located within the apparatus of the mitral valve, including the base of the anterior mitral leaflet in 3; and in another patient with endocarditis in a native mitral valve, the abscess was found in the posterior papillary muscle. Two patients with aortic-valve endocarditis had abscesses in both the aortic root and interventricular septum.

Transthoracic Echocardiography

On transthoracic echocardiography only 13 of the 46 abscesses (28.3 percent) could be correctly identified; most were abscesses at the aortic root (their location is listed in Table 1). Evaluation of the transthoracic studies by the two independent observers revealed initial discrepancies in 4 of the 118 patients (3.4 percent): 3 of the 4 had an abscess of the aortic root (1 of them with prosthetic-valve endocarditis), and 1 had an abscess in the interventricular septum complicating endocarditis in a native aortic valve.

In one patient, transthoracic echocardiography resulted in a false positive diagnosis of abscess; in this patient, an abscess around a prosthetic mitral valve was suspected but could not be confirmed on surgery. Transthoracic echocardiography thus had a sensitivity of 28.3 percent, a specificity of 98.6 percent, and positive and negative predictive values of 92.9 and 68.9 percent, respectively, in diagnosing abscesses associated with endocarditis.

Transesophageal Echocardiography

As compared with the transthoracic approach, transesophageal echocardiography allowed a significantly higher rate of detection of abscesses associated with endocarditis (P<0.001): 40 of the 46 abscesses documented by surgery or autopsy (87 percent) were correctly identified. Table 1 shows the rates of detection according to the location of the abscess, and typical examples are shown in Figures 1Figure 1Transesophageal Echocardiogram of a Patient with Aortic-Valve Endocarditis. through 4. In 26 of the 44 patients with abscesses documented by surgery or autopsy (59.1 percent), abscesses were missed by transthoracic echocardiography but correctly identified by the transesophageal procedure. No patient had an abscess detected by transthoracic echocardiography alone.

In five patients, independent evaluation by two observers resulted in initial discrepancies, amounting to an interobserver variability of 4.2 percent: four patients had endocarditis of a native aortic valve with an abscess of the aortic root (three patients) or interventricular septum (one patient); the fifth patient had a mitral prosthetic endocarditis without abscess at surgery. The interobserver variability of transthoracic and transesophageal echocardiography was not significantly different.

In four patients (including the patient with a false positive diagnosis on transthoracic echocardiography), evaluation of the transesophageal images resulted in a false positive diagnosis of abscess. In one patient with endocarditis of a native aortic valve, a small abscess of the interventricular septum was diagnosed echocardiographically, and in three patients with endocarditis of a mitral valve (two native and one prosthetic), ring abscesses suspected on echocardiography could not be confirmed during surgery. The two patients with infected native mitral valves also had sclerotic changes of the annular region, and all four false positive diagnoses were made in the first half of the consecutive series of patients. For the detection of abscess, the transesophageal approach had a sensitivity of 87 percent, a specificity of 94.6 percent, and positive and negative predictive values of 90.9 and 92.1 percent, respectively.

Clinical Data

The clinical characteristics of the patients with endocarditis-associated abscesses and those without are shown in Table 2Table 2Clinical Characteristics of 44 Patients with Endocarditis-Associated Abscesses Found during Surgery or at Autopsy and 74 Patients without Such Abscesses.. There were no significant differences in age and sex between the two groups. Abscesses were significantly more frequent, however, in patients with aortic-valve endocarditis than in those with nonaortic-valve infection (37 of 78 [47.4 percent] vs. 14 of 59 [23.7 percent], P<0.01). In patients with abscess, staphylococcus was found significantly more often than other infecting organisms (52.3 vs. 16.2 percent, P<0.001). Blood cultures were negative in 31 of the 118 patients; the majority of these patients had been referred from other hospitals and had previously received antibiotic therapy. Patients with prosthetic-valve infections had a slightly higher percentage of abscesses than those with endocarditis of a native valve (17 of 34 [50 percent] vs. 34 of 103 [33 percent]), and the percentage of hospital deaths was higher in the group with abscesses than in the group without (22.7 vs. 13.5 percent); these differences did not reach the level of significance.

Discussion

Infective endocarditis is still a life-threatening disease; to initiate appropriate therapy, early diagnosis is essential. Whereas echocardiography is recognized as the method of choice for the detection of valvular vegetations associated with endocarditis,1 2 3 4 the detection of endocarditis-associated abscesses by the transthoracic approach is difficult. The early identification of abscesses complicating infective endocarditis is particularly important, however, since in patients with such abscesses, antibiotic therapy may not be able to penetrate the areas of abscess effectively. It has been proposed that surgery before widespread tissue destruction has occurred may improve outcome.28

Previous Echocardiographic Studies

Most of the echocardiographic experience concerning the diagnosis of abscesses associated with endocarditis is based on case reports; data on larger series of patients are scarce. Saner et al. reported on nine patients with aortic-valve endocarditis in whom abscesses of the aortic root were identified by two-dimensional transthoracic echocardiography.16 Since only patients with echocardiographically detected abscesses were included, however, the study offered no conclusions on the reliability of echocardiographic identification of abscesses. Byrd et al. used similar selection criteria.18

Ellis et al.11 studied 46 patients with infective endocarditis documented by surgery or autopsy – 22 patients with associated abscesses and 24 without. On the basis of study results, the authors recommended four diagnostic criteria for two-dimensional (transthoracic) echocardiographic diagnosis of abscesses: prosthetic-valve rocking, aneurysm in the sinus of Valsalva, thickness of the anterior or posterior wall of the aortic root ≥10 mm, and perivalvular density in a septum ≥ 14 mm. The presence of one or more of these criteria had positive and negative predictive values for the detection of abscess of 86 and 87 percent, respectively. Most of the abscesses in the study (18 of 22) were located at the aortic root, however, and the authors correctly pointed out that all these abnormalities can be observed in many diseases other than abscesses associated with endocarditis.11 , 29 30 31 32 In addition, none of the four criteria alone had sufficient clinical reliability for abscess detection. In the present study the echocardiographic definition of an abscess was therefore restricted to a definite region of reduced echo density or echolucency.

Transesophageal Echocardiography in the Present Study

We used transesophageal echocardiography in addition to the conventional transthoracic approach. Many clinical indications for the use of transesophageal echocardiography have been documented during the past few years,33 , 34 and the indications are further evolving and expanding. Although the transesophageal technique is associated with some minor discomfort to the patient, it provides high-quality images of the heart and thoracic aorta in virtually all patients, because the close anatomical proximity of the esophagus to the heart allows unobstructed views of most cardiac and great-vessel anatomy. Transesophageal echocardiography can also be performed with a higher-frequency transducer than the transthoracic procedure, and image resolution is markedly improved. Finally, transesophageal echocardiography carries a low risk when it is performed by an experienced operator.35 , 36

This study shows that abscesses associated with endocarditis, when defined as regions of reduced echo density or echolucency, can be detected more often by the transesophageal than by the transthoracic approach. Whereas the specificity and positive predictive value of the two techniques are similar, the sensitivity and negative predictive value of the transesophageal method are remarkably higher.

Limitations of the Study

The fact that only patients with endocarditis documented during surgery or at autopsy were included in this study could be viewed as a limitation. Patients who had echocardiographic examinations but did not go on to have histologic and macroscopic confirmation were not included. This fact could affect both the positive and the negative predictive accuracy of the transthoracic and transesophageal tests. However, the selection criteria in this study provided the only way to avoid uncertainty about whether an abscess had been correctly identified.

The fact that the surgeons were aware of the echocardiographic findings in most cases, which may have influenced the intraoperative detection of abscesses, may be considered a further limitation. This potential bias is unavoidable, however, and any other procedure would be unethical; surgeons need complete information on the morphologic and functional status of the heart before they operate. Furthermore, the diagnosis of abscess was based not only on direct intraoperative inspection but also on histopathological examination.

The diagnosis of vegetative lesions and associated abscesses by transthoracic echocardiography is difficult in patients with prosthetic valves or annular or valvular sclerotic or calcific changes. Although transesophageal echocardiography may allow an easier diagnosis of valvular vegetations in such patients, diagnosing abscesses remains difficult. Three of the four false positive diagnoses on transesophageal echocardiography in our series were made in patients with a prosthetic valve or annular calcification. In particular, a small abscess in the region of the right coronary sinus can be missed in patients with a mechanical device in the aortic position, because of acoustical shadowing.

Although one could argue that performing a transthoracic examination before the transesophageal study improved the diagnostic accuracy of the transesophageal approach, in routine clinical settings transthoracic echocardiography should always be performed before the transesophageal procedure. The two techniques complement one another and are not competitive. In addition, in 26 of the 44 patients in our study with abscesses documented by surgery or autopsy, transthoracic studies produced false negative results and were therefore misleading in the evaluation of the transesophageal images.

Clinical Implications

This study documents that transesophageal echocardiography, in addition to its demonstrated superiority over the transthoracic approach in the visualization of vegetations, improves the rate of detection of abscesses associated with endocarditis. Since patients with infected native or prosthetic valves usually have a worse prognosis when they have associated abscesses than when they do not, this feature of the transesophageal technique is of direct prognostic and therapeutic relevance. Patients with identified abscesses in the clinical setting of infective endocarditis are usually candidates for more aggressive therapy (including early surgery) than those without abscesses. In the present series, all 44 patients with abscesses either required surgery because of advanced heart failure or persistent infection, or died before operation. We therefore believe that patients who have a prolonged clinical course of infective endocarditis (in particular, persistent signs of infection) and those who do not respond to adequate medical therapy, as well as patients with persistent fever early after valve replacement, should undergo a transesophageal echocardiographic examination.

Presented in part at the 59th Annual Scientific Sessions of the American Heart Association, Dallas, November 17—20, 1986.

We are indebted to Miss R. Schützenmeister for excellent technical assistance in the echocardiographic laboratory.

Source Information

From the Division of Cardiology, Department of Internal Medicine (W.G.D., A.M., O.L., D.H., B.N.-D., P.R.L.), and the Department of Thoracic and Cardiovascular Surgery (J.L.), Hannover Medical School, Hannover, Germany; and the Division of Cardiology, Emory University School of Medicine, Atlanta (R.P.M.). Address reprint requests to Dr. Daniel at the Division of Cardiology, Department of Internal Medicine, Hannover Medical School, Konstanty-Gutschow-Str. 8, D-3000 Hannover 61, Germany.

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