Subepicardial adipose tissue producing echocardiographic appearance of pericardial effusion

MISCELLANEOUSTOPICS

Subepicardial Adipose Tissue Producing Echocardiographic Appearance of Pericardial Effusion Documentation by Computed Tomography and Necropsy

JEFFREY M. ISNER, MD, BARBARA L. CARTER, MD, WILLIAM C. ROBERTS, MD, and MARK S. BANKOFF, MD

An isolated anterior echo-free space is generally regarded as a false-positive echocardiographic finding for pericardial effusion. Even when an anterior echo-free space is accompanied by a posterior echo-free space, the echo-free spaces have been occasionally reported to be falsely positive for pericardial effusion, principally in patients with cardiac neoplasms. The basis for these findings has

never been adequately explained, in the present study, evaluation by computed tomographic imaging or necropsy examination of 5 patients in whom there was either an anterior or posterior echo-free space or both demonstrated that subepicardial adipose tissue is the echocardiographic imitator of pericardial effusion.

Methods Computed tomographic imaging of

The presence by cardiac ultrasound of an anterior echo-free space in the absence of a posterior echo-free space represents a combination of findings known to imitate, b u t seldom indicate, a pericardial effusion./, 2 Although speculated to result from subepicardial adipose tissue,l,3, 4 an isolated anterior echo-free space has never been established with c e r t a i n t y to result from subepicardial fat. T h e present r e p o r t documents by necropsy examination in 1 patient and computed tomographic imaging of the chest in 2 other patients t h a t subepicardial adipose tissue is the basis for the finding of an isolated anterior echo-free space. F u r t h e r m o r e , .necropsy findings and results of computed t o m o g r a p h y m 2 additional patients suggest t h a t subepicardial adipose tissue is the basis for echocardiograms previously reported as being falsely positive for pericardial effusion in patients with a cardiac neoplasm.

t h e c h e s t was p e r -

formed on a Siemen's Somatom-2 whole body scanner that utilizes a rotating gantry. A complete section scan with a slice thickness of 8 mm was performed in 5 seconds using 125 kV and 46 mA. At least 2 separate windows of varying contrast were viewed at each level. The scale for transparency was -1,000 Hounsfield Units (HU) for air, 0 for water, and +1,000 HU for bone; the attenuation coefficient for any given site was determined by multiple cursor sampling. M-mode echocardiography was performed on either a Smith-Kline or Unirad ultrasonoscope with a 2.55 MHz transducer. Particular care was taken to prevent directing the ultrasonic beam too far medially. A switched-gain ("damping") mechanism 5 was used to evaluate the pericardial space in each patient. Two-dimensional real-time echocardiography was performed with either a mechanical (Hoffrel 201) or phased array (Hewlett-Packard) sector scanner. Pertinent clinical and necropsy findings in the 4 patients are summarized in Table I and in Figures I to 6.

Discussion

From the Departments of Medicine (Cardiology) and Radiology, TuftsNew EnglandMedical Center, Boston, Massachusetts; and the Pathology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland. Manuscript received and accepted August 13, 1982. Address for reprints: Jeffrey M. Isner, MD, Box 70, New England Medical Center, 171 Harrison Avenue, Boston, Massachusetts 02111.

Although the finding of an echo-free space posterior to the left ventricular free wall has come to represent the echocardiographic sine qua non for pericardial effusion, the initial description of the use of ultrasound for diagnosing pericardial effusion involved an isolated echo-free space anterior to the right ventricular free

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FIGURE 1. M-mode echocardiogram from Patient 1 shows an isolated anterior echo-free space (Ant EFS) anterior to the right ventricular free wall (RVFW). Chest computed tomogram shows that the echo-free space is due to subepicardial fat interposed between the pericardium (Peri) and right ventricle (RV). AML = anterior mitral leaflet; Ant = anterior; Ao = aorta; ecg = electrocardiogram; L = left; I_VFW = left ventricular free wall; Post = posterior; R = right; VS = ventricular septum.

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wall. 6 Subsequently, Feigenbaum et al 7,8 demonstrated that the extent of pericardial fluid accumulation must be quite large before an anterior echo-free space is observed, so that it is nearly always associated with a posterior echo-free space. In fact, an anterior echo-free space in the absence of a posterior echo-free space was one of the earliest patterns to be recognized as a falsepositive finding in the echocardiographic diagnosis of pericardial effusion. 1 Horowitz et al 2 suggested that such an isolated anterior echo-free space might result from either fibrous tissue or lung interposed between the heart and anterior chest wall. Teichholz 9 suggested that in addition to connective tissue and lung, adipose tissue might be responsible for separating the anterior wall of the right ventricle from the chest wall. Feigenbaum 3 agreed that epicardial fat was the most likely basis for the finding of an anterior echo-free space. While the admonitions of these and other investigators established that the finding of (1) an anterior echo-free space in the absence of a posterior echo-free space is an inadequate diagnostic criterion for the presence of a pericardial effusion, and (2) that the basis for such an isolated anterior

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FIGURE 2. Patient 2. The anterior echo-free space on an M-mode echocardiogram was due to extensive subepicardial adipose tissue, greater over the anterior right ventricle (RV) than the posterior left ventricle (LV). AML = anterior mitral leaflet; Ant EFS = anterior echo-free space; ecg = electrocardiogram; Endo = endocardium; OMI = old myocardial infarction; VS = ventricular septum.

echo-free space was likely to be epicardial fat, documentation of the latter has not been previously established. The present study establishes by computed tomographic imaging and necropsy examination that the isolated anterior echo-free space is in fact due to the anterior epicardial fat.

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~o FIGURE 3. M-mode echocardiogram (top panel) from Patient 3 shows anterior (Ant) and posterior (Post) echo-free space (EFS). A "sweep" from left ventricle to left atrium showed no echo-free space posterior to the left atrium. At necropsy, gross examination of the heart (bottom left panel) disclosed no pericardial fluid. Instead, extensive subepicardial fat was interposed between underlying myocardium and metastatic bronchogenic carcinoma. The latter encased the heart in a nearly circumferential manner. Photomicrograph (bottom right panel) shows tumor, fat, and underlying myocardium (Myo). (Movat's pentachrome stain; original magnification X 6), reduced 3 8 % . ecg = electrocardiogram; LV = left ventricle; MV = mitral valve; RV = right ventricle; VS = ventricular septum.

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FIGURE 4, Hemodynamic recordings from Patient 3. The mean right atrial (RA), right ventricular (RV) end-diastolic, and mean pulmonary capillary wedge (PCWP) pressures are equal. The RA phasic trace (top left) has an M-shaped contour with a steep y descent. The RV pressure contour has an initial dip, followed by a short end-diastolic (ed) plateau. These hemodynamic findings documented constrictive/restrictive physiology secondary to tumor encasement of the heart, ecg = electrocardiogram.

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B.O. 5/12 FIGURE 5. M-mode echo and computed tomographic scan from Patient 4. The M-mode echocardiogram shows an anterior relatively echo-free space (Ant EFS). Chest computed tomogram shows this to be due to fat underlying the pericardium (Peri); the pericardium itself is thickened by presumed metastatic bronchogenic carcinoma. The posterior echo-free space was related to the pleural effusion (Pleural Eft) seen on computed tomography. Ant = anterior; ecg = electrocardiogram; L = left; MV = mitral valve; Post = posterior; R = right; RVFW = right ventricular free wall; VS = ventricular septum.

The amount of subepicardial fat generally increases with age. l° These deposits are characteristically most extensive over the anterior portion of the heart--in contrast to the posterior heart--a fact which explains the propensity for extensive subepicardial fat to produce an anterior echo-free space in the absence of a posterior echo-free space. While the extent of the fat is not necessarily related to the adipose content of other body tissues, the extent of subepicardial fat tends to be greater in obese individuals; 4 of our 5 patients were in fact obese (Table I). Endogenous or exogenous steroid excess (for example, long-term administration of high-dose steroid therapy) constitutes another setting in which an increased amount of subepicardial fat is commonly seen. 11 This factor may have played a role in the excessive amount of subepicardial adipose tissue in Patients 2 and 5 (Table I). The unique capabilty of computed tomography to identify relative tissue density makes this diagnostic technique ideal for determining the basis of relatively sonolucent spaces visualized by cardiac ultrasound. 12 The relatively low attenuation coefficient of fat (-60 to -100 HU) established with certainty that the isolated anterior echo-free space in Patients 1 and 5 was due to subepicardial fat. A similar echocardiographic finding in Patient 2 was confirmed at necropsy. Although necropsy examination in the latter patient was performed over 1 year after the last M-mode echocardiogram, the absence of any posterior echo-free space on any of the multiple echocardiograms recorded and the finding at necropsy of normal visceral and parietal pericardia suggest that the anterior echo-free space resulted from the excessive amount of fat seen at necropsy rather than a transient pericardial effusion. In Patients 1, 2, and 5, the characteristically greater distribution of fat over the anterior, as opposed to the posterior, surface of the heart resulted in an isolated anterior echo-free space by car-

diac ultrasound. In Patients 2 and 5, a small amount of posteriorly located fat appeared to result in a small posterior echo-free sliver with the boundary lines moving in parallel during systole and diastole. The finding of an anterior echo-free space that is out of proportion to an associated posterior echo-free space is therefore a valuable clue to the possibility that such echo-free spaces represent fat rather than fluid. In contrast to the finding of an isolated anterior echo-free space, the finding of an isolated posterior echo-free space, provided it persists through ventricular diastole as well as systole, has been shown to be a reliable indicator of pericardial effusion.2 As mentioned above, the finding of an anterior echo-free space in combination with a posterior echo-free space generally indicates a large effusion.2,%s Even in the situation in which both an anterior and posterior echo-free space are observed together, however, echocardiograms may be falsely positive for a pericardial effusion, particularly as the result of a cardiac neoplasm. 13-16 The explanation for this association is poorly understood. In the patient reported by Lin et al, 15the false-positive echo-free space seen anteriorly and posteriorly was attributed to the type of neoplasm encasing the heart (angiosarcoma with a rich vascular component). Millman et a113 described 3 patients with metastatic carcinoma or lymphoma in whom a sonolucent space posterior to the left ventricle was unassociated with pericardial effusion at operation or necropsy. These authors also attributed the echo-free space to the neoplasm itself, suggesting that the acoustic impedence of the neoplasm might be the same as that of pericardial fluid. Come et a116 reported 3 patients with metastatic tumor involving the pericardium. All 3 had a posterior echo-free space and 2 had both anterior and posterior echo-free spaces. In 1 patient, a 62year-old man with lymphoma encasing the heart in whom there was both an anterior and posterior echo-

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Necropsy findings and examination by computed tomographic imaging in Patients 3 and 4, respectively, demonstrate that subepicardial fat is the basis for the ability of neoplasms encasing the heart to simulate pericardial effusion on cardiac ultrasound. In Patient 3, generalized obesity was associated with extensive subepicardial fat that completely encased the heart, before superimposed encasement by metastatic bronchogenic carcinoma. The nearly circumferential deposits of subepicardial adipose tissue and the obliteration of the nonfluid filled pericardial cavity at necropsy demonstrate that fat was the basis for the echo-free space on this patient's echocardiogram. The tumor in this patient further simulated pericardial heart disease by causing physiologic constriction, a finding observed previously in patients with cardiac encasement by metastatic neoplasm. 14 In Patient 4, the capability of computed tomography to accurately identify tissue density again demonstrated that subepicardial adipose tissue interposed between encasing metastatic bronchogenic carcinoma and underlying myocardium was the basis for the echo-free space in this patient's Mmode and 2-dimensional echocardiograms. Finally, the results of this computed tomographic and necropsy study suggest that caution must be observed in evaluating relatively sonolucent spaces in elderly obese patients who have no clinical evidence of pericardial heart disease. Findings in Patients 1, 4, and 5 also underscore the utility of computed tomography in clarifying the basis of an apparent echo-free space on cardiac ultrasound examination in patients in whom the finding is either unexpected or contrary to available clinical information. References

FIGURE 6. M-mode echocardiogram and computed tomographic scan from Patient 5. a and b, M-mode echocardiograms at 2 different gain settings each show an anterior (Ant) relatively echo-free space (EFS) anterior to the right ventricular free wall (RVFW). c, M-mode echocardiographic " s w e e p " from the left ventricular free wall (LVFW) to the left atrium (LA) shows a small posterior (Post) echo-free space in addition to an anterior echo-free space, d, computed tomographic scan shows that an anterior space on the M-mode echocardiogram is due to extensive subepicardial fat anterior to the right ventricle (RV), while a small posterior echo-free space is due to a small amount of fat posterolateral to the left ventricle (LV). AML = anterior mitral leaflet; Ao = aorta; ecg = electrocardiogram; L = left; Peri = pericardium; R = right; VS = ventricular septum.

free space, " . . . the epicardial fat pad was seen to lie several centimeters within the anterior heart border on the lateral film." In a second patient with metastatic ,s,quamous cell carcinoma, the posterior echo-free space • •. was seen only at the junction of the left atrium and left ventricle...," that is, the atrioventricular sulcus where deposits of adipose tissue are generally extensire.

1. Feigenbaum H. Ultrasound diagnosis of pericardial effusion. First World Congress of Ultrason=cDiagnostics in Medicine, Vienna, June, 1969. Vienna Academy of Medicine Publishing Department. Chest 1969;55:59-62. 2. Horowilz MS, Schultz CS, Stinson EB, Harrison DC, Popp RL. Sensitivity and specificity of echocardiographic diagnosis of pericardial effusion. Circulation 1974;50:239-247• 3. Feigenbaum H. Echocardiography. 3rd ed Philadelphia: Lea & Febiger, 1981:478-504. 4. Ellis K, King DL. Pencarditis and pericardial effusion: radiologic and echocardlographic diagnosis. Radiol Clin North Am 1973; 11:393-413. 5, Grlffith JM, Henry WL. Switched gain: a technique for simplifying ultrasonic measurement of cardiac wall thickness. IEEE Trans Biomed Eng 1975; 22:337-340. 6, Edler I. Diagnostic use of ultrasound in heart disease. Acta Med Scand 1955;308:32-36. 7, Feigenbaum H, Waldhausen JA, Hyde LP. Ultrasound diagnosis of pericardial effusion• JAMA 1965;191:107-110 8. Feigenbaum H. Echocardiographic diagnosis of pericardial effusion. Am J Cardiol 1970;26:475-479. 9. Teichholz LE. Echocardiographic evaluation of pericardlal diseases. Prog Cardiovasc Dis 1978;21:133-140. 10. Roberls WC, Spray TL. Pericardial heart disease. Curt Probl Cardiol 1977;2:1-71. 11. Bulkley BH, Roberts WC. The heart in systemic lupus erythematosus and the changes induced in it by corticosteroid therapy. A study of 36 necropsy patients. Am J Med 1975;58:243-264. 12. Isner JM, Carter BL, Benkoff, MS, Konslam MA, Salem DN, Computed tomography in the diagnosis of pericardial heart disease Ann Intern Med 1982;97:373-379 13. Millman A, Meller J, Motto M, Blank HF, Horowitz I, Herman MV, Teicholz LE. Pericardial tumor or fibrosis mimicking pericardial effusion by echocardiography. Ann Intern Med 1977;85:434-436. 14. Foote WC, Jefferson CM, Price HL. False-positive echocardiographic diagnosis of pericardial effusion• Result of tumor encasement of the heart simulating constrictive pericardltis Chest 1977;71:546-549. 15. Lin TK, Stech JM, Eckert WG, Lin JJ, Farha SJ, Hagan CT. Perlcardial angiosarcoma simulating pericardial effusion by echocardiography. Chest 1978;73:881-883. 16. Come PC, Riley MF, Fortuin NJ. Echocardiographic mimicry of pericardial effusion• Am J Cardiol 1981;47:365-370•