Pericardial effusion diagnosed by reflected ultrasound

Pericardial Effusion Diagnosed by

Reflected Ultrasound*

JACK J. KLEIN, M.D. and BERNARD L. SEGAL, M.D., F.A.C.C.

Philadelphia, Pennsylvania

T HE USE of reflected ultrasound in the diagnosis of perieardial effusion has been the

subject of many reports from numerous in- stitutions since 1965.im5 These reports suggest that by means of this technic pericardial effusion can be diagnosed with a high degree of accuracy. The results of animal experimentation in our laboratory and in others have shown that as little as 50 cc. of fluid within the pericardium can be found ultrasonically.lt5

We have now examined posterior wall motion by reflected ultrasound in over 200 patients (Fig. 1). Pericardial effusion was found in 30 patients. We report our technic and correlate these ultrasonic findings with the results obtained by 1311 albumin scan, pericardiocentesis, surgical exploration of the pericardium and necropsy studies.

MATERIAL AND METHOD The cause of pericardial effusion in the 30 patients

is shown in Table I. In Group A (19 patients), we were able to confirm the ultrasonic findings by either pericardiocentesis, i:‘iI albumin scan, surgical exploration, necropsy studies, or a combination of these technics. The patients in Group A were all clinically diagnosed as having pericardial effusion because of pericardial friction rub, large cardiac silhouette, low voltage noted on the electrocardiogram, or a rapidly changing heart size. At least two of these findings were noted in each patient.

The patients in Group B all had diseases frequently associated in our experience with pericardial effusion and were studied for that reason, even though 4 patients (Cases 22, 25, 28 and 29) did not present clinical evidence of effusior.. The 4 were found by reflected ultrasound to have small collections of fluid in the posterior pericardial sac. Three patients (Cases 23, 24 and 26) who had uremia and were on a chronic renal hemodialysis program were studied before and

after each dialysis. Two (Cases 21 and 27) were in congestive heart failure and showed good clinical evidence of pericardial effusion. One (Case 30) presented classical evidence of acute pericarditis and another (Case 20) presented with vague chest pain and was found by reflected ultrasound to have a small anterior pericardial effusion on one occasion and a posterior effusion subsequently. The latter case also emphasizes the fact that a small effusion is often missed by 13iI albumin scan.

An Ekoline-20 Mark II ultrasonoscope equipped with “A” and “B” modes for presentation of reflected ultrasonic energy and a single electrocardiographic lead, which served as a timing device, was used in these studies. Self-developing film was employed for permanent recording of the images shown on the cathode ray tube of the ultrasonoscope.

Figure 1. Normal motion of the posterior wall in a patient without pericardial effusion. The electrocardiogram (ECG) is also shown.

* From the Cardiology Section, Department of Medicine, Hahnemann Medical College and Hospital, Philadelphia, Pa. This investigation was supported in part by Public Health Service Grant HE 09937-01 and by the Cassett Founda- tion.

Address for reprints: Bernard L. Segal, M.D., Department of Medicine, Hahnemann Medical College and Hospital, 230 N. Broad St., Philadelphia, Pa. 19102.

VOLUME 22, JULY 1’368 57

Klein and Segal

TABLE I

Data on Thirty Patients with Pericardial Effusion

Case Age/ Confirma- NO. Sex Etiology ti0n

Group A. ConJrmation Without Ultrasound

1 67/F

2 61/M

3 56/F

4 64/F 5 43/M

6 35/M 7 35/F 8 60/M

9 33/F 10 62/F

11 45/F

12 13

60/F 61/F

14 70/M

15 46/M

16 23/M 17 29/F 18 32/M 19 44/F

Group B. Confrmation by Ultrasound Only

Chronic effusive pericarditis

Acute myocardial infarction; rupture left ventricle

Chronic effusive pericarditis

Hypothyroidism Amyloid cardiomyop-

athy Uremia Viral pericarditis Congestive heart fail-

ure Uremia Congestive heart fail-

ure Congestive heart fail-

ure Malignant effusion Congestive heart fail-


ure Hodgkins disease in

pericardium Acute pericarditis Uremia Malignant effusion Congestive heart fail-

Scan, centesis

Autopsy

Scan, surgery, autopsy

Scan Scan, autopsy

Autopsy Scan Scan

Scan Scan

Scan

Scan Scan

Autopsy

Centesis

Scan Scan Scan, centesis Scan

20 48/M

21 67/F

22 39/M

23 20/F

24 41 /M

25 47/F

26 16/M 27 62/M

28 57/M

29 60/M 30 50/M

Chronic pericarditis

Congestive heart failure

Acute rheumatoid ar- thritis

Uremia

Uremia

Congestive heart failure

Uremia Congestive heart fail-


ure Uremia Acute pericarditis

Serial echo, scan neg.

Serial echo

Serial echo

Pre- & post- dialysis echo

Pre- & post- dialysis echo

Serial echo

Serial echo Serial echo

Serial echo

Serial echo Serial echo

Our technic was similar to that of Feigenbaum et al.’ The controls on the ultrasonoscope were adjusted to permit maximal clarity of those echoes reflected from the posterior wall of the left ventricle and the pericardium. The ultrasonic transducer was hand- held at the fourth or fifth left interspace near the lateral sternal border (with slight lateral and inferior angulation). Medial angulation of the transducer frequently produced ultrasonic reflections from the mitral valve. It is generally accepted that medial angulation of the transducer can produce false positive results because the ultrasonic beam may encounter the mitral annulus and nonmoving mediastinal structures or the vertebral column lying immediately behind the heart.

When a large pericardial effusion was present, the ultrasonic technic was reliable despite slight variations in the position of the transducer. In these patients with large effusions, separation between the posterior wall and pericardium could be found at more than one position. Small effusions of 100 to 200 cc. could be found most easily at the fourth or fifth intercostal space adjacent to the lateral border of the sternum. This transducer position generally would be in a line with the posteroinferior aspect of the pericardial sac, where small amounts of nonloculated fluid initially accumulate.

RESULTS

The 19 cases reported in Group A include a wide variety of causes of pericardial effusion. The “B” presentation trace and the 1311 albumin scan in Case 4 are shown in Figure 2. In this case, despite evidence of a large pericardial effusion by both methods, ultrasound did not demonstrate a separation of echoes between the anterior heart wall and the pericardium. As a rule, effusions were diagnosed far more frequently by checking for an echo separation between the posterior wall and pericardium.2 An echo separation found anteriorly helped confirm the diagnosis most often in cases of large pericardial effusion. In only 1 patient (Case 20, Group B) with chronic pericarditis was an effusion more easily found anteriorly than posteriorly (Fig. 3). The effusion may have been loculated anteriorly in this case.

In 3 cases in Group A echocardiographic findings that indicated pericardial effusion in patients with uremia and were confirmed by 1311 albumin scan disappeared after hemodialysis and subsequently returned in the days after the dialysis procedure. On the basis of these findings we were able to find four addi- tional examples of pericardial effusion in such patients which were not diagnosed by other methods. In these cases, serial studies by re-

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Pericardial Effusion Diagnosed by Reflected Ultrasound 59

Figure 2. Case 4. “B” presentation trace (B) and the isi1 albumin scan (A) are seen side by side. Anterior wall motion (AW) is noted at the top of the picture. There does not appear to be a significant separation b,etween the AW and pericardium. The posterior wall (PW) is separated from the pericardium (P). The lung (L) is labeled immediately behind the pericardium.

Figure 3. Case 20. Note the clear separation between pericardium (P) and anterior wall (AW). This particular photograph of the “B” presentation does not show the usual separation between the posterior wall and pericardium which was present on other traces.

fleeted ultrasound before hemodialysis showed a pericardial effusion. After hemodialysis the effusion disappeared (Fig. 4).

In 1 patient (Cas,e 1) the diagnosis of pericardial effusion was confirmed by scan, ultrasound and pericardiocentesis. A total of 700 cc. of fluid was removed while simultaneous ultrasonic determinations were being taken (Fig. 5). This has been done previously in only 1 reported case.3 The distance between the echoes

VOLUME 22, JULY 1968

from the posterior wall and those from the pericardium changed only slightly after the removal of 475 cc. This finding agrees with observations of Soulen et a1.,3 who indicated that fluid shifts occur during the tap. We believe that the nonloculated fluid located anteriorly and laterally gradually shifts into the more dependent portions of the pericardial sac, thus preventing a significant reduction in the distance between the posterior wall and the pericardium until the last 200 to 300 cc. are removed. This finding was used to our advantage when we encountered difficulty in continuing to aspirate fluid after removal of only several hundred cubic centi- meters. In this case, evidence of fluid remain- ing in the pericardial sac suggested that change of the patient’s position might increase the yield of fluid. Reflected ultrasound indicated when the effusion was completely aspirated, thereby precluding further unnecessary taps and avoid- ing the need for repeated chest x-ray examina- tions.

In reviewing our cases, we have found two examples of unequivocal false positives. The first example was that of a patient with calcific constrictive pericarditis. Figure 6 shows what appears to be a classic anterior pericardial effusion without a significant posterior effusion. At operation, this patient was found to have an organized thrombus anteriorly between the calcified pericardium and the anterior wall of the heart. The acoustically homogeneous thrombus interposed between the anterior wall and the pericardium was diagnosed ultrasonically as effusion.

Another false positive study was found in an

60 Klein and Segal

Figure 4. Case 23, Group B. These traces were taken before (A) and after (B) hemodialysis. Note the separation between AW and PW and P. The effusion has disappeared after hemodialysis.

elderly man admitted with congestive heart failure due to severe rheumatic valvular disease. Reflected ultrasound showed a 3 cm. separation between the echoes of the posterior wall and the pericardium. At necropsy, the patient’s hyper- trophied posterior wall measured 3 cm. from endocardium to epicardium, suggesting that what was measured was the thickness of the

posterior wall rather than pericardial effusion (Fig. 7). We have since become interested in the ultrasonic measurement of posterior wall thickness and find that our preliminary results correlate well with direct measurement of posterior wall thickness at necropsy. More work is now being conducted in our laboratory to evalu- ate the reliability of this measurement.

Figure 6. A false positive result was obtained (not listed in Table I) when we interpreted the separation between AW and P as an indica- tion of pericardial effusion. At operation, a homogeneous thrombus was found separating the calcified pericardium from the anterior wall.

Figure 7. The false positive results in this case (not listed in Table I) resulted from assuming that the separation between the two structures indicated pericardial effusion. At autopsy, the waveform at 15 cm. was found to be endocardium (END). The structure without motion at 18 cm. is epicardium (EPI). The wall was 3 cm. thick by direct measurement.

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Pericardial Effusion Diagnosed by Reflected Ultrasound

Figure 5. Case 1: Group A. This is a composite of the “B” presentation traces taken during pericardiocentesis. Note that despite the removal of 475 cc. of fluid the separation between PW and P persists. In this case, anterior wall motion (AW) is also separated from echoes reflected from the chest wall and anterior pericardium (not labeled). Note that the separation between echoes from AW and the structures anterior to it gradually dis- appears as the effusion is with- drawn. This indicates that fluid recedes into the more dependent and posterior portions of the pericardium preservin,? the separation between PW and P.

DISCUSSION

In the past two years, published reports have emphasized that the use of reflected ultrasound as an aid in the diagnosis of pericardial effusion is a simple and convenient bedside procedure. The accuracy of this procedure has been high, although the limited number of cases reported thus far is not adequate to establish definitely the degree of accuracy. The accuracy of the procedure is definitely enhanced by the skill and experience of the operator performing the test. False positive results or misinterpretation of results should become less frequent as experience


with this technic increases. It is also possible that reflected ultrasound will enable us to detect much smaller collections of fluid than any of the other procedures at present available. We have shown experimentally that 50 cc. of effusion will be demonstrated in the dog.” About 100 to 200 cc. of nonloculated effusion can be found ultrasonically in our patients. The 1311 albumin scan probably does not possess this accuracy.6-8 A small chronic effusion is, in gen- eral, not hemodynamically significant, but an acute effusion of 200 cc. may produce cardiac tamponade. The detection of a small effusion is important because it permits an earlier diagnosis

62 Klein and Segal

of pericarditis, postmyocardial infarction syn- drome, or traumatic rupture of the heart secon- dary to chest trauma or perforation by an intra- cardiac catheter.

Degree of Separation of Posterior Wall and Peri- cardium in Pericardial E&ion: Clinically, we have not been able to correlate accurately the amount of pericardial effusion with the degree of echo separation between the posterior wall and the pericardium. Even under the better controlled conditions of our dog experiments, a disparity existed between the amount of effusion and the degree of separation.5 In our experience, the finding of an echo separation between the anterior wall of the heart and the pericardium generally indicates a large effusion.

Friction Rub in th Presence qf Pericardial Efusion: It is generally accepted that the disappearance of a pericardial friction rub indicates the presence of a pericardial effusion. This is contra- dicted by our findings that a collection of fluid located in the dependent or posterior part of the sac can exist in the presence of a friction rub that is probably generated in the anterior or lateral portions of the pericardial sac where fluid does not separate the structures. The patients with uremic pericarditis and a loud friction rub were found to have a significant pericardial effusion. Sufficient fluid must accumulate in the pericardial sac to separate the heart and pericardium on all sides to eliminate a friction rub.

Changes in Cardiac Position with Various Degrees of Pericardial Ejusion: We have already indicated that pericardial fluid collects in the dependent portions of the sac. This was first found in our dog experiments, in which we were able to visualize directly the fluid collecting in the dependent portion of the pericardial sac when an effusion was experimentally created. As more fluid was infused into the pericardium, this fluid diffused laterally and then anteriorly. The heart was displaced anteriorly with the initial infusion of 50 to 100 cc. Clinically, in the patient whose simuItaneous uhrasonic exam- inations were performed during pericardiocentesis, the heart did not sink posteriorly until the removal of the last 300 cc. of effusion. This observation suggests that the fluid present anteriorly and laterally shifted into the dependent areas of the pericardial sac during the removal of the initial 350 to 400 cc., thus maintaining a fixed distance between the echoes from the posterior wall and the pericardium.

Reflected ultrasound has repeatedly shown

that with drainage of the perirardial effusion the posterior pericardium moves no more than 5 mm. anteriorly because the pericardium is anchored to the mediastinum, diaphragm and chest wall. The spinal column limits posterior displacement.

Cardiac Motion Occurring with Pericardial Eju- sion: Feigenbaum et al9 were able to document excessive cardiac motion during different stages of pericardial effusion in 6 patients. Of the 6, 4 had pericardial effusions associated with invasion of the pericardium by malignant tumor. We can add 2 cases of pericardial effusion owing to malignant neoplasms to this group. Prior to pericardiocentesis, the motion of the anterior wall was excessive and in the same direction as the motion of the posterior ventricular wall (Fig. 8). After removal of the fluid, the motion of both walls was less conspicuous. Normally the anterior and pos-

Figure 8. Case 12. This “B” presentation trace taken from a patient with metastatic tissue in the pericardium indicates a large pericardial effusion separating the anterior and posterior walls of the heart from the pericardium. The two walls move unexpectedly in the same direction rather than in opposite directions. An- terior wall motion (AW) is increased. Motion of the heart in an anteroposterior direction could be responsible for the increased anterior wall excursion as well as the continuous motion of both walls in the same direction. Sufficient effusion was present in this case to separate the heart walls from the pericardium, thus per- mitting unrestrained motion of the heart.

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Pericardial Effusion Diagnosed by Reflected Ultrasound 63

terior ventricular walls move in opposite directions during each phase of the cardiac cycle. Of the possible explanations proposed by Feigenbaum and other authors,‘O the most likely seem to be those associating the growth of malignant tissue with a rigid pericardium. As a result of such growth the pericardium is fixed and indistensible so that the existing effusion as well as any further effusion is uniformly distributed throughout the pericardial sac. The uniform distribution of fluid within the pericardial sac would aid cardiac motion by preventing contact between the pericardium and the heart.

An in vitro model was developed to simulate cardiac motion in the presence of a large pericardial effusion. Ultrasound recordings were taken of the model in motion and were found to resemble those showing the exaggerated motion of tE.e heart in the presence of a malignant pericardial effusion (Fig. 9).

Figure 9. This “B” presentation was taken from a model developed to simulate the heart surrounded by a large pericardial effusion. The anterior simulated pericardium is labeled AB and the posterior simulated pericardium, PB. The simulated heart walls are labeled AW for anterior wall and PW for posterior wall. Note the exaggerated motion of the walls in addition to the continuous motion of both walls in one direction. The model heart in this example was noted to be swinging in an anteroposterior direction during the simulated phases of the cardiac cycle.


Rejected C’ltrasound As an Aid During Peri- cardiocentesis: Reflected ultrasound may be used at the bedside during pericardiocentesis. In our patient, reflected ultrasound indicated that a significant amount of fluid remained in the pericardium even though the surgeon had indicated his inability to aspirate more fluid. The patient assumed a more upright position, and another 400 cc. of fluid was removed. This eliminated the necessity of pro- viding stand-by x-ray equipment or moving the patient to the x-ray department.

False Posit&e Results: We were able to demonstrate in Figure 6 that homogeneous thrombus separating the anterior pericardium from the anterior myocardium was mistakenly diagnosed as anterior pericardial effusion. Any homogeneous material that separates the pericardium from the myocardium, whether it be fluid, tumor, or thrombus, can be misinterpreted by reflected ultrasound. Ultrasound is reflected at tissue interfaces or, in other words, by a change in the physical characteristics of a medium.

The myocardium presents an endocardial and an epicardial echo-reflecting surface. When significant thickening of the myocardium oc- curs, the echoes reflected from these two sur- faces can be misinterpreted as pericardial effusion. We have now been able to measure the thickness of the myocardium regularly by using a modification of our technic for diagnosing pericardial effusion.

We believe that detecting the presence of lung echoes behind the posterior wall echo is helpful in determining that the transducer is being angled laterally enough to avoid making ultrasound contact with the vertebral column or the paraspinal muscles. Such contact can be misinterpreted as a prominent nonmoving echo behind the posterior wall echo.

SUMMARY

This paper presents an evaluation of the use of reflected ultrasound in the detection of pericardial effusion in 30 patients. The patients were divided into two groups. Group A consisted of 19 patients whose effusion was confirmed by another 11 patients, had serial formed to confirm the effusion.

Two patients with a of pericardial effusion

procedure. Group B, ultrasonic studies per- presence of pericardial

false positive diagnosis are included, and the

64 Klein and Segal

reasons for the faulty diagnoses are discussed. Our evaluation of this technic suggests

that reflected ultrasound can be used to diag- nose pericardial effusions of smaller amounts than other technics now widely used.

The technic also appears to be of great help during pericardiocentesis in that it can quickly tell the clinician whether the fluid has been completely removed or if a change in the direction of the needle or position of the patient will increase the yield of fluid.

ACKNOWLEDGMENT

We thank Dr. Millard (3011 of the Department of Radiology of Hahnemann Medical College and Hos- pital for his assistance in evaluating the Is’1 albumin scans used in this paper.

REFERENCES

1. FEIGENBAUM, H., WALDHAUSEN, J. A. and HYDE, H. P. Ultrasound diagnosis of pericardial effusion. J.A.M.A., 191: 107, 1965.

2. FEIGENBAUM, H., ZAKY, A. and WALDHAUSEN, J. A. Use of ultrasound in the diagnosis of pericardial

effusion. Ann. Int. Med., 65: 443, 1966. 3. SOULEN, R. H., HAPAYOROKER, M. S. and GIMENEG,

J. H. Echocardiography in the diagnosis of pericardial effusion. Radiology, 86: 1047, 1966.

4. Moss, A. .I. and BRUHN, F. The echocardiogram; an ultrasound technic for the detection of pericardial effusion. New England J. Med., 247: 380, 1966.

5. KLEIN, .I. J., RABER, G., SHIMADA, H., KINGSLEY, B. and SEGAL, B. L. Evaluation of induced pericardial effusion by reflected ultrasound. Am. J.

Cardiol., 22: 49, 1968. 6. BONTE, F. J., ANDREWS, G. J., ELMENDORF, E. A.,

PRESLEY, N. H. and KROHMER, J. S. Radioiso- tope scanning in the detection of pericardial effusions. South. M. J., 55: 577, 196i.

7. WAGNER. H. N.. MCAFEE. J. G. and MOZLEY. J. M. Diagnosis of pericardiai effusion by radioisotope scanning. Arch. Znt. Med., 108: 679, 1961.

8. CHARLES, N. D. and SKLAROFF, D. M. Radioiso- tope scanning as a diagnostic aid in cardiovascular disease. J.A.M.A., 186: 920, 1963.

9. FEIGENBAUM, H., ZAKY, A. and GRABHORN, H. H. Cardiac motion in patients with pericardial effusion. Circulation, 34: 611, 1966.

10. LITTMANN, D. Alternation of the heart. Circulation, 27: 280, 1963.

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Pericardial effusion diagnosed by reflected ultrasound