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Evaluation of induced pericardial effusion by reflected ultrasound
Experimental
Studies
Evalualtion of Induced Pericardial
Effusion
by Reflected Ultrasound* JACK J. KLEI;V,
M.D., GEORGE RABER, HIDEYO SHIMADA, M.D., BENEDICT KINGSLEY, M.SC. and BERNARD L. SEGAL, M.D., F.A.C.C. Philadelphia,
Pennsylvania
freeing the side not operated on for ultrasonic evaluation of cardiac motion. Preoperative and postoperative control traces of posterior wall motion were taken. A constant transducer position was maintained with a ringstand and clamps at the dog’s fourth left intercostal space along the parasternal border (Fig. 1). Saline solution was infused into the pericardium in increments of 25 cc. Photographs of the “B” presentation made with the use of self-developing film were taken after each increment. When cardiac tamponade occurred, the fluid was removed in increments of 50 cc., and photographs were taken.
HE DIAGNOSIS of pericardial effusion by reflected ultrasound is well established and has been termed an accepted bedside procedure. Edler’ in 1954 described a separation of echoes between the anterior wall of the heart and the pericardium in a patient with pericardial effusion. Feigenbaum et a1.2 in 1965 reported their experimental and clinical findings on the ultrasonic diagnosis of pericardial effusion and were able to verify their findings in 5 dogs in which they had created pericardial effusion. This paper reports a similar study and in addition provides information on the ultrasonic reflecting characteristics of the posterior wall, pericardium and the lung.
T
MAI,ERIAL AND METHOD Seven mongrel dogs weighing on the average approximately 23 kg. were anesthetized with Dial urethane (0.6 cc./kg.Il and ventilated through an endotracheal tube connected to a positive pressure respirator. The right hemithorax was entered through the fourth or fifth intercostal space. A PE-190 catheter was inserted into the pericardial sac near the atrioventricular groove and advanced cephalad or caudad approximately 5 cm. [t subsequently became apparent that only those catheters inserted in the cephalad direction functioned without tearing the pericardium. The catheter was, firmly sutured to the pericardium. The chest was closed and the pneumothorax relieved. The dog was then positioned on the right side, thus
Figure 1. The ultrasonic transducer is shown mounted with a ringstand and clamps at the dog’s fourth left interspace near the sternum.
* 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 Foundation. Address for reprints: Bernard L. Segal, M.D., Department of Medicine, Hahnemann Medical College and Hospital, 230 N. Broad St., Philadelphia, Pa. 19102.
VOLUME22,
JULY 1968
49
50
Klein et al.
The animals were then sacrificed and examined. In 5 dogs a calibrated needle was inserted into the chest through both anterior and posterior left ventricular walls in the line of the ultrasonic beam (Fig. 2). The chest was then opened at an adjacent interspace. Measurements of distances and anatomic In 2 sacrificed dogs ultrarelations were recorded. sonic examination was performed on the closed chest at the fourth left interspace and also with the sensor applied directly over the fluid-filled pericardium. An Ekoline-20 Mark II Ultrasonoscope was used for these experiments. It was equipped with a transducer (diameter 19 mm.) producing 1,000 The pulses/set. at a frequency of 2.25 megacycles. apparatus had both “A” and “B” modes for presentation of the returning echoes and a standard electrocardiographic lead for timing. The apparatus was equipped with both reject and gain controls to provide maximal definition for returning echoes. The intensity-modulated “B” presentation coupled with a vertical slow sweep produced a distinct waveform of posterior wall motion. In this way motion of a cardiac structure over a period of time could be evaluated (Fig. 3).
AW
EGG
PW
i&&G
“A” and “B” modes for the presentation of reflected echoes are shown below the drawing of the chest. The “A” mode presents each echo as a spike on a horizontal
Figure 3.
Figure 2. The dog’s chest is shown opened at the fourth left interspace. The needle was inserted through the closed chest in the path of the ultrasonic beam. The chest was subsequently opened without removing the needle. The needle is shown to pass through the anterior wall of the left ventricle (LV). The left atria1 appendage (LAA) is noted superiorly. The right ventricle (RV) is noted to the left of the interventricular groove and the left anterior descending artery (LAD).
range scale (range scale not shown). Distance of the structure from the transducer is measured on the range scale. The spikes oscillate in a horizontal direction, thereby reflecting the motion of the ventricular walls. The “B” mode shows each spike converted into an intensity-modulated dot. The brightness of the dot is an indication of the amount of reflected energy from a The dots, swept vertically across the screen, structure. produce the waveforms of anterior wall (AW) and the posterior wall (PW) motion. The lung is shown on “ES” presentation as a series of linear or random streaks. A = atrium, MV = mitral valve, Ao = aorta, and LV = left ventricle. THE
AMERICAN
JOURNAL
OF
CARDIOLOGY
Reflected
Ultrasound
and
RESULTS
Posterior Wall Motion: The control echoes of posterior wall motion taken before and after thoracotomy showed only a minimal change in the distance between transducer and the wall. These changes were attributed to the effects of the thoracotomy. The normal posterior wall
Control Pre-00
Ant.
Pericardial
F
ll
150 cc In.
B.
C.
PM F
m
Withdrowina -125 cc remoin
51
moved between 0.5 to 1.0 cm. (Fig. 4A). Angulation of the transducer before it was permanently mounted tended to vary the configuration and amplitude of the waveform slightly, but the relation of the posterior wall motion to the QRS complex remained unchanged. The initial motion of the posterior wall during systole was anterior and toward the transducer.
50 cc In.
A.
Effusion
Withdrowino -75cc
remain
F
Control wst-effusion
F
Figure 4. Composite of traces from dog No. 7 showing the development of the pericardial effusion and its subsequent withdrawal. A, the control preoperative trace was taken before the animal was operated on. The posterior wall (PW) is found Note the waveform of PW motion and its correlation with the QRS 9 cm. from the transducer or anterior chest wall. The PW moves anteriorly just after the inscription of the QRS. of the electrocardiogram (ECG). B, after 50 cc. of saline solution was infused, the PW is separated from the pericardium (P). The relatively echofree area between them is the effusion (EFF). Note also that the pericardium moves slightly anteriorly synchronously PM’ has moved anteriorly about 1 cm. (see text), and P has moved posteriorly about 0.5 cm. with the PW. C, with 150 cc. of saline infused, there has been no significant change in the separation between PW and P (see text). The cardiac rate has increased as an indication of the increased pressure in the pericardial sac. The pericardial motion is decreased as a a result of increased intrapericardial pressure. D, withdrawal of the effusion leaving 125 cc. within the pericardium slows the cardiac rate and increases the pericardial motion slightly but does not change the distance between PW and P. E, withdrawal of saline to 75 cc. causes further slowing of the cardiac rate with a slight change in the appearance of PW motion but no significant change in the separation between PW and P. The PW has moved posteriorly to 8.5 cm. F, removal of all the saline shows the waveform of PW alone.
VOLUME22, JULY 1968
Klein
52
Structures in front of and behind the posterior The mitral valve wall reflect ultrasonic energy. and its valve ring may be located in the field of the ultrasonic beam. Generally, the transducer was angled in a direction to avoid these structures. Studies employing a long calibrated needle show that the ultrasonic beam usually enters the left ventricle anteriorly and below the mitral valve, and exits through the left ventricle posteriorly4 (Fig. 5). The lung envelops the left ventricle posteriorly, laterally and anterolaterally. Those echoes reflected from structures behind the posterior wall of the left ventricle are “B” presentation of pulmonary origin (Fig. 4). of these echoes appears as a series of random dots or streaks. Separation of the Posterior Wall and Pericardial In the dogs with an Echoes in Pericardial Effusion: intact pericardium a separation between the posterior wall and the pericardium occurred after 50 cc. of saline solution was infused (Fig. 6A). This became such a reliable finding that it was 50 cc In.
125
et al.
Figure 5. Needle inserted into heart in the direction of the ultrasound beam. The needle enters the anterior wall (AW) of the left ventricle (LV) and passes into the left ventricular cavity near the base of the anterior papillary muscle. It traverses the ventricular cavity below the leaflets of the mitral valve (MV) and exits through the posterior wall (PW).
cc In
ECG PW P
possible to infer that the pericardium was leaking Figure 6B shows if a separation did not occur. an example of lack of separation even with an inThe conclusion that fusion of 125 cc. of saline. no pericardial effusion existed was supported bythe necropsy results, which demonstrated a hole in the apical area of the pericardial sac. In each animal an attempt was made to infuse sufficient saline to cause cardiac tamponade. This was manifested by a reduction in blood pressure and an increase in heart rate, and generally occurred after infusion of 200 cc. Slight nonlinear, progressive separation of the echoes from the posterior wall and pericardium developed as the amount of pericardial fluid increased (Fig. 4). This seemed to be the result
Figure 6. A, the separation between PW and P with an infusion of 50 cc. is a very reliable indication of pericardial effusion noted in multiple experiments (see Fig. 4). B, although 125 cc. of saline was infused into the pericardium, no separation between PW and P appeared. Pericardial effusion The fluid escaped is not present. from the pericardium.
of anterior displacement of the heart rather than posterior displacement of the pericardium. As expected, the saline collected in the dependent portion of the pericardial sac. As intrapericardial pressure was increased by the further infusion of saline, the fluid distribution was more uniform, but the dependent portion still held the most fluid. Thus, the heart tended to be displaced anteriorly toward the sensor. Motion of the Anterior Wall of the Left Ventricle: During this series of experiments, attempts were made to record the motion of the anterior wall. Two transducers were used, one 19 mm., 2.25 mc. and the other 5 mm., 7.75 mc. The smaller transducer fit easily between ribs but was not powerful enough to record anterior wall motion THE AMERICANJOURNAL
OF CARDIOLOGY
Reflected Control
Pm-op
Ultrasound 95
and Pericardial
Effusion
cc In
PH
Figure 7. A, the erldocardial (END) and epicardial (EPI) interfaces of the posterior wall (PW) are clearly seen in this trace. The endocardial interface is brighter or more dominant. The PW measures 8 mm. in thickness from the top of the waveform of the endocardium to the top of the waveform of the epicardium. B, the same dog was sacrificed (note ventricular fibrillation on the electrocardiogram). A pericardial effusion (EFF) of 95 cc. is present. Note that the endocardial interface (END) is more dominant than the epicardial interface (EPI) and both are of less intensity than the pericardial interface. The reject and gain controls have been readThe PW is 8 mm. thick as noted in A. justed to obtain an optimal picture. C, the transducer was placed on the surface of the anterior pericardium of the same dog and aimed posteriorly. Note that those echoes arising from the endccardium are more dominant than those arising from epicardium. The echo-free area is pericardial effusion (EFF). The pericardium (P) is slightly more dominant than endocardium.
Figure (EFF.) pleural seen in cardium
8. A, both pericardial (under arrowhead) and effusions (PE) can be this picture. The periis separated on both
sides by echo-free areas in-j dicating fluid. B, no pericardial effusion :d to be separated from lung (L) . of fluid leaked from the pericardium pericardial waveform. without a significantly loss of ultrasonic energy due to the overlying lung tissue. When the standard 19 mm. transducer was used, anterior wall motion was noted, but anterior and posterior wall motion could not be recorded simultaneously without varying the gain controls. Reflecting Characteristics of Cardiac Interfaces: One dog was sacrificed to compare echoes arising from the posterior wall and pericardium during life with those from the same structures after death (Fig. 7, A to C). The endocardial surface of the left ventricle was a dominant reflecting surface during life and death. Examination of the tracings taken in vivo revealed separate and discrete echoes from the endocarVOLUME
22,
JULY
1968
dial and epicardial surfaces of the posterior ventricular wall, those of the epicardial surface being of lesser intensity. After sacrifice these interfaces were also noted to have similar reflecting characteristics. The thickness of the posterior wall could be measured in vivo, and the measurement compared favorably with those taken after death by ultrasound and with a calibrated needle. The transducer was then applied directly over the fluid-filled pericardium. The endocardium was again found to produce the dominant echo from the posterior wall (Fig. 7C). The ultrasonic reflections from the pericardium were equal to or slightly greater than those from the posterior wall.
Klein
et al.
A. NORMAL
PWPEP
PERiCARDlAL EFFUSION
Figure 9.
Right venticular (RV) and intrapericardial recorded simultaneoudy. As right (IP) pressures ventricular pressure rises during contraction, the intrapericardial pressure falls. The reduction in intrapericardial pressure correlated with the pericardial motion noted on the “B” presentation as shown in Figure 4.
Pericardial Effusion and Pleural Effusion: During the infusion of saline into the pericardium, leakage developed, as already described. It was noted that the “B” presentation photographs taken during these experiments revealed a relatively echo-free area on both sides of the Leakage from the pericardium (Fig. 8A). pericardium was confirmed by direct visualization of the fluid in the pleural cavity at necropsy. In effect, the pericardium was isolated on both sides by fluid. This finding is considered additional evidence that the pericardium contributes in large part to the dominant echo behind the posterior wall during pericardial effusion. In 1 dog there was total leakage of fluid into the pleural cavity, and autopsy proved that no pericardial effusion existed. Even though pulmonary and posterior wall echoes were separated, this finding was not consistent with pericardial effusion because the dominant echo of the pericardium was absent from its expected position immediately anterior to the echoes arising in the lungs (Fig. 8B). Relation of Intrapericardial Pressure to Motion of the Posterior Wall and Pericardium: When no pericardial effusion exists the pericardial motion is indistinguishable from that of the heart. When the two structures are separated by fluid, each structure has its own identifiable waveform. The waveform of the posterior wall remains the same until the intrapericardial pressure becomes markedly elevated, at which time the amplitude of the waveform may decrease.
L
c. ~R~AR#~~ AND PLEURAL EFFUStONS
PW Pl.E
L
0.
.
Figure
10.
Summary
of all of the findings.
A, normal posterior waI1 (PW) motion in the absence effusion. Th e random dots behind the of pericardial PW are lung (L) echoes. B, in the presence of pericardial effusion (PE) posterior wall and pericardial (P) echoes are separated by an echo-free area.
C, the addition of pleural effusion (P1.E) shows an echo-free area on both sides of the dominant pericardial echoes. D, pleural effusion can be differentiated from pericardial effusion if the dominant waveform of pericardium is not present between PW and lung (L).
THE
AMERICAN
JOURNAL
OF CARDIOLOGY
Reflected
Ultrasound
The pericardium during the infusion of saline is not always without motion. During ventricular contraction the intrapericardial pressure falls, and the pericardium actually moves slightly about 2 mm. in the same direction as the posterior ventricular wall (Fig. 4 and 9). DISCUSSION These experiments lend additional support to the reliability of reflected ultrasound in the diagnosis of perica:rdial effusion. The anatomic separation that develops between the posterior wall and the pericardium with pericardial effusion is diagnosed ultrasonically by observing the characteristic waveforms on both structures recorded by the “13” presentation. The typical waveform of posterior wall motion is identified visually whether or not pericardial effusion exists. The timing of posterior wall motion is accomplished through the use of a simultaneous electrocardiogram. The initial motion of the posterior wall is anterior immediately after the QRS complex on the electrocardiogram. During diastole the wall moves in a posterior direction away from the transducer.5 These experiments have improved our understanding of the reflecting characteristics of cardiac interfaces. The dominance of reflected echoes from an interface in the heart depends on several factors. Reflected ultrasonic energy is determined by a change in the acoustic resistance of a tissue at an interface. Acoustic resistance is defined as the product of tissue density and velocity of sound in the same medium (pV) .6 When the ultrasonic beam passes from blood to endocardium, epicardium to fluid to pericardium (if pericardial effusion exists), reflected energy is returned to the transducer from each of these interfaces. If the structure has a smooth, flat surface located perpendicular to the direction of the ultrasonic beam and exhibits little or no motion it should reflect a maximal amount of ultrasonic energy. In the case of pericardial effusion, the pericardial echoes are dominant, probably because the pericardium is smoother and less curved and remains relatively stationary. Reflected energy arising from the pericardium appears more dominant than that arising from the endocardial surface of the left ventricle. This finding is caused by the changing curvature of the contracting wall in relation to the relative lack of motion of the fluid-filled pericardium. Also, because of its trabeculations, the endocardium VOLUME
22,
JULY
1968
and Pericardial
Effusion
55
presents an irregular surface to the ultrasonic beam. Motion of the posterior wall tends to scatter ultrasonic energy. The reasons for the lack of dominance of those echoes reflected from the epicardial surface of the posterior wall require further investigation. Additional evidence to support the conclusion that the pericardium is responsible for the dominant waveform during pericardial effusion was gained when fluid escaped from the pericardial sac during the experiment. The pericardium was then noted to be separated from the posterior wall and lung by fluid. The random echoes returned from the lung were distinguishable from those arising in the pericardium. No distinct waveform could be ascribed to the lung echoes.7 Furthermore, we now believe that pericardial effusion may be differentiated clinically from pleural effusion with the aid of these criteria. The absence of pericardial echoes interposed between the waveform of posterior wall and the random echoes of lung enable us to infer the presence of pleural effusion. Pleural effusion without pericardial effusion was subsequently confirmed after the animal was sacrificed (Fig. 10). The pericardium moved no more than 2 mm. during ventricular contraction because the changes in pressure were minimal in ~ the pericardial sac. The simultaneous recording of intrapericardial and right ventricular pressure revealed that intrapericardial pressure dropped during ventricular contraction. The relation between changes in intrapericardial pressure and pericardial motion is now being investigated. These experiments also furnished evidence that measurement of the thickness of the left ventricular posterior wall can be accomplished ultrasonically. Comparing the measurements taken by ultrasound with those made by using a long calibrated needle inserted through the myocardium revealed identical measurements. fhiM.kRY
An experimental evaluation of the ultrasonic technic. for the diagnosis of pericardial effusion revealed the following: 1. The individual waveforms of posterior wall and pericardium could be differentiated after as little as 50 cc. of saline solution was infused into the pericardium. The waveform of the posterior wall could be quickly identified. When pericardial effusion existed the waveform
Klein
56
et al.
of the posterior wall was separated by an echofree area from the waveform of the pericardium. 2. The pericardium is capable of reflecting more ultrasonic energy than the posterior ventricular wall. 3. Pleural effusion can probably be differentiated from pericardial effusion. 4. The major interface of the left ventricular posterior wall is the blood-endocardium interface. The distance from the blood-endocardium to the epicardium-fluid or lung interface is a measure of wall thickness which compares favorably with direct measurements taken at autopsy.
REFERENCES 1. EDLER, I.
Diagnostic use of ultrasound in heart disease. Acta med. scandinav., 308 (Suppl.): 32,
1955. 2. FEIGENBAUM,H., WALDENHAUSEN,J. A. and HYDE,
3.
4.
5.
6.
ACKNOWLEDGMENT
7.
Dr. Klein thanks Dr. Harvey Feigenbaum for permission to visit his laboratory and observe his technic for evaluating pericardial effusion.
DRUGS 29
cardiac
Dqmseallta
32424 Autonomic Drug-
L. P. Ultrasound diagnosis of pericardial effusion. J.A.M.A., 191: 107, 1965. SEGAL, B. L., LIKOFF, W. L. and KINGLSEY, B. Echocardiography: Clinical application in mitral stenosis. J.A.M.A., 195: 161, 1966. EDLER, I., GUSTAFSON, A., KARLEFORS, T. and CHRISTENSSON,B. Ultrasoundcardiography. Acta med. scandinav., 370 (Suppl.): 9, 1961. FEIGENBAU~~, H., ZAKY, A. and WALDHAUSEN,J. A. Use of ultrasound in the diagnosis of pericardial effusion. Ann Int. Med., 65: 443, 1966. KINSLER, L. E. and FREY, A. R. Fundamentals of Acoustics, chap. 8. New York, 1962. John Wiley & sons. JOYNER, C. R., HERMAN, R. J. and REID, J. M. Reflected ultrasound in the detection and localization of pleural effusion. J.A.M.A., 200: 129. 1967.
IN USE 4/68 - 16441
u 5019/l95
pro~anolol mm
. Aftar 10 mg. &WI isoprenallns up to 10 r&liz over 24 hrs. ; After 2nd 5 qg. dose
Malea No. Patients
Dossge:init.l0mg. then 2.5 & 5 me. dosms
no effect except
A. Good recovexy. B. Gradually improved recovered.
i~~prsasll~ 4 ak/min. give1 with little effect. ardioversion performed ulth reversion to sinus rhythm. soprezmline incr. to l5~g/ll&n* with170 *of sodim bicarbonate over nsxt 3 hrs. for presumptive lactic acidos%s.
pigastric pain, & ther bowel movement with
...proprsnolol in small oral doses may cause profound shock and ~reatitis in susceptible hdividuale; and the amount of isoprenaline required to counteract the effect...is far greater than that ususlly used." Taylor, J.A. (Kaiser Found. Hosp., San F'IWIC~SCO,Calif. Q-potenslon after orsl prO~mOl01. Lancet 1: 532-533 (Mar. 9) I368 [Lettsrs to Editor] Prepared by Paul de Haen, Inc. for the drug index card system,
“de Haen Drugs in Use.” THE AMERICANJOURNAL OF CARDIOLOGY
Studies
Evalualtion of Induced Pericardial
Effusion
by Reflected Ultrasound* JACK J. KLEI;V,
M.D., GEORGE RABER, HIDEYO SHIMADA, M.D., BENEDICT KINGSLEY, M.SC. and BERNARD L. SEGAL, M.D., F.A.C.C. Philadelphia,
Pennsylvania
freeing the side not operated on for ultrasonic evaluation of cardiac motion. Preoperative and postoperative control traces of posterior wall motion were taken. A constant transducer position was maintained with a ringstand and clamps at the dog’s fourth left intercostal space along the parasternal border (Fig. 1). Saline solution was infused into the pericardium in increments of 25 cc. Photographs of the “B” presentation made with the use of self-developing film were taken after each increment. When cardiac tamponade occurred, the fluid was removed in increments of 50 cc., and photographs were taken.
HE DIAGNOSIS of pericardial effusion by reflected ultrasound is well established and has been termed an accepted bedside procedure. Edler’ in 1954 described a separation of echoes between the anterior wall of the heart and the pericardium in a patient with pericardial effusion. Feigenbaum et a1.2 in 1965 reported their experimental and clinical findings on the ultrasonic diagnosis of pericardial effusion and were able to verify their findings in 5 dogs in which they had created pericardial effusion. This paper reports a similar study and in addition provides information on the ultrasonic reflecting characteristics of the posterior wall, pericardium and the lung.
T
MAI,ERIAL AND METHOD Seven mongrel dogs weighing on the average approximately 23 kg. were anesthetized with Dial urethane (0.6 cc./kg.Il and ventilated through an endotracheal tube connected to a positive pressure respirator. The right hemithorax was entered through the fourth or fifth intercostal space. A PE-190 catheter was inserted into the pericardial sac near the atrioventricular groove and advanced cephalad or caudad approximately 5 cm. [t subsequently became apparent that only those catheters inserted in the cephalad direction functioned without tearing the pericardium. The catheter was, firmly sutured to the pericardium. The chest was closed and the pneumothorax relieved. The dog was then positioned on the right side, thus
Figure 1. The ultrasonic transducer is shown mounted with a ringstand and clamps at the dog’s fourth left interspace near the sternum.
* 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 Foundation. Address for reprints: Bernard L. Segal, M.D., Department of Medicine, Hahnemann Medical College and Hospital, 230 N. Broad St., Philadelphia, Pa. 19102.
VOLUME22,
JULY 1968
49
50
Klein et al.
The animals were then sacrificed and examined. In 5 dogs a calibrated needle was inserted into the chest through both anterior and posterior left ventricular walls in the line of the ultrasonic beam (Fig. 2). The chest was then opened at an adjacent interspace. Measurements of distances and anatomic In 2 sacrificed dogs ultrarelations were recorded. sonic examination was performed on the closed chest at the fourth left interspace and also with the sensor applied directly over the fluid-filled pericardium. An Ekoline-20 Mark II Ultrasonoscope was used for these experiments. It was equipped with a transducer (diameter 19 mm.) producing 1,000 The pulses/set. at a frequency of 2.25 megacycles. apparatus had both “A” and “B” modes for presentation of the returning echoes and a standard electrocardiographic lead for timing. The apparatus was equipped with both reject and gain controls to provide maximal definition for returning echoes. The intensity-modulated “B” presentation coupled with a vertical slow sweep produced a distinct waveform of posterior wall motion. In this way motion of a cardiac structure over a period of time could be evaluated (Fig. 3).
AW
EGG
PW
i&&G
“A” and “B” modes for the presentation of reflected echoes are shown below the drawing of the chest. The “A” mode presents each echo as a spike on a horizontal
Figure 3.
Figure 2. The dog’s chest is shown opened at the fourth left interspace. The needle was inserted through the closed chest in the path of the ultrasonic beam. The chest was subsequently opened without removing the needle. The needle is shown to pass through the anterior wall of the left ventricle (LV). The left atria1 appendage (LAA) is noted superiorly. The right ventricle (RV) is noted to the left of the interventricular groove and the left anterior descending artery (LAD).
range scale (range scale not shown). Distance of the structure from the transducer is measured on the range scale. The spikes oscillate in a horizontal direction, thereby reflecting the motion of the ventricular walls. The “B” mode shows each spike converted into an intensity-modulated dot. The brightness of the dot is an indication of the amount of reflected energy from a The dots, swept vertically across the screen, structure. produce the waveforms of anterior wall (AW) and the posterior wall (PW) motion. The lung is shown on “ES” presentation as a series of linear or random streaks. A = atrium, MV = mitral valve, Ao = aorta, and LV = left ventricle. THE
AMERICAN
JOURNAL
OF
CARDIOLOGY
Reflected
Ultrasound
and
RESULTS
Posterior Wall Motion: The control echoes of posterior wall motion taken before and after thoracotomy showed only a minimal change in the distance between transducer and the wall. These changes were attributed to the effects of the thoracotomy. The normal posterior wall
Control Pre-00
Ant.
Pericardial
F
ll
150 cc In.
B.
C.
PM F
m
Withdrowina -125 cc remoin
51
moved between 0.5 to 1.0 cm. (Fig. 4A). Angulation of the transducer before it was permanently mounted tended to vary the configuration and amplitude of the waveform slightly, but the relation of the posterior wall motion to the QRS complex remained unchanged. The initial motion of the posterior wall during systole was anterior and toward the transducer.
50 cc In.
A.
Effusion
Withdrowino -75cc
remain
F
Control wst-effusion
F
Figure 4. Composite of traces from dog No. 7 showing the development of the pericardial effusion and its subsequent withdrawal. A, the control preoperative trace was taken before the animal was operated on. The posterior wall (PW) is found Note the waveform of PW motion and its correlation with the QRS 9 cm. from the transducer or anterior chest wall. The PW moves anteriorly just after the inscription of the QRS. of the electrocardiogram (ECG). B, after 50 cc. of saline solution was infused, the PW is separated from the pericardium (P). The relatively echofree area between them is the effusion (EFF). Note also that the pericardium moves slightly anteriorly synchronously PM’ has moved anteriorly about 1 cm. (see text), and P has moved posteriorly about 0.5 cm. with the PW. C, with 150 cc. of saline infused, there has been no significant change in the separation between PW and P (see text). The cardiac rate has increased as an indication of the increased pressure in the pericardial sac. The pericardial motion is decreased as a a result of increased intrapericardial pressure. D, withdrawal of the effusion leaving 125 cc. within the pericardium slows the cardiac rate and increases the pericardial motion slightly but does not change the distance between PW and P. E, withdrawal of saline to 75 cc. causes further slowing of the cardiac rate with a slight change in the appearance of PW motion but no significant change in the separation between PW and P. The PW has moved posteriorly to 8.5 cm. F, removal of all the saline shows the waveform of PW alone.
VOLUME22, JULY 1968
Klein
52
Structures in front of and behind the posterior The mitral valve wall reflect ultrasonic energy. and its valve ring may be located in the field of the ultrasonic beam. Generally, the transducer was angled in a direction to avoid these structures. Studies employing a long calibrated needle show that the ultrasonic beam usually enters the left ventricle anteriorly and below the mitral valve, and exits through the left ventricle posteriorly4 (Fig. 5). The lung envelops the left ventricle posteriorly, laterally and anterolaterally. Those echoes reflected from structures behind the posterior wall of the left ventricle are “B” presentation of pulmonary origin (Fig. 4). of these echoes appears as a series of random dots or streaks. Separation of the Posterior Wall and Pericardial In the dogs with an Echoes in Pericardial Effusion: intact pericardium a separation between the posterior wall and the pericardium occurred after 50 cc. of saline solution was infused (Fig. 6A). This became such a reliable finding that it was 50 cc In.
125
et al.
Figure 5. Needle inserted into heart in the direction of the ultrasound beam. The needle enters the anterior wall (AW) of the left ventricle (LV) and passes into the left ventricular cavity near the base of the anterior papillary muscle. It traverses the ventricular cavity below the leaflets of the mitral valve (MV) and exits through the posterior wall (PW).
cc In
ECG PW P
possible to infer that the pericardium was leaking Figure 6B shows if a separation did not occur. an example of lack of separation even with an inThe conclusion that fusion of 125 cc. of saline. no pericardial effusion existed was supported bythe necropsy results, which demonstrated a hole in the apical area of the pericardial sac. In each animal an attempt was made to infuse sufficient saline to cause cardiac tamponade. This was manifested by a reduction in blood pressure and an increase in heart rate, and generally occurred after infusion of 200 cc. Slight nonlinear, progressive separation of the echoes from the posterior wall and pericardium developed as the amount of pericardial fluid increased (Fig. 4). This seemed to be the result
Figure 6. A, the separation between PW and P with an infusion of 50 cc. is a very reliable indication of pericardial effusion noted in multiple experiments (see Fig. 4). B, although 125 cc. of saline was infused into the pericardium, no separation between PW and P appeared. Pericardial effusion The fluid escaped is not present. from the pericardium.
of anterior displacement of the heart rather than posterior displacement of the pericardium. As expected, the saline collected in the dependent portion of the pericardial sac. As intrapericardial pressure was increased by the further infusion of saline, the fluid distribution was more uniform, but the dependent portion still held the most fluid. Thus, the heart tended to be displaced anteriorly toward the sensor. Motion of the Anterior Wall of the Left Ventricle: During this series of experiments, attempts were made to record the motion of the anterior wall. Two transducers were used, one 19 mm., 2.25 mc. and the other 5 mm., 7.75 mc. The smaller transducer fit easily between ribs but was not powerful enough to record anterior wall motion THE AMERICANJOURNAL
OF CARDIOLOGY
Reflected Control
Pm-op
Ultrasound 95
and Pericardial
Effusion
cc In
PH
Figure 7. A, the erldocardial (END) and epicardial (EPI) interfaces of the posterior wall (PW) are clearly seen in this trace. The endocardial interface is brighter or more dominant. The PW measures 8 mm. in thickness from the top of the waveform of the endocardium to the top of the waveform of the epicardium. B, the same dog was sacrificed (note ventricular fibrillation on the electrocardiogram). A pericardial effusion (EFF) of 95 cc. is present. Note that the endocardial interface (END) is more dominant than the epicardial interface (EPI) and both are of less intensity than the pericardial interface. The reject and gain controls have been readThe PW is 8 mm. thick as noted in A. justed to obtain an optimal picture. C, the transducer was placed on the surface of the anterior pericardium of the same dog and aimed posteriorly. Note that those echoes arising from the endccardium are more dominant than those arising from epicardium. The echo-free area is pericardial effusion (EFF). The pericardium (P) is slightly more dominant than endocardium.
Figure (EFF.) pleural seen in cardium
8. A, both pericardial (under arrowhead) and effusions (PE) can be this picture. The periis separated on both
sides by echo-free areas in-j dicating fluid. B, no pericardial effusion :d to be separated from lung (L) . of fluid leaked from the pericardium pericardial waveform. without a significantly loss of ultrasonic energy due to the overlying lung tissue. When the standard 19 mm. transducer was used, anterior wall motion was noted, but anterior and posterior wall motion could not be recorded simultaneously without varying the gain controls. Reflecting Characteristics of Cardiac Interfaces: One dog was sacrificed to compare echoes arising from the posterior wall and pericardium during life with those from the same structures after death (Fig. 7, A to C). The endocardial surface of the left ventricle was a dominant reflecting surface during life and death. Examination of the tracings taken in vivo revealed separate and discrete echoes from the endocarVOLUME
22,
JULY
1968
dial and epicardial surfaces of the posterior ventricular wall, those of the epicardial surface being of lesser intensity. After sacrifice these interfaces were also noted to have similar reflecting characteristics. The thickness of the posterior wall could be measured in vivo, and the measurement compared favorably with those taken after death by ultrasound and with a calibrated needle. The transducer was then applied directly over the fluid-filled pericardium. The endocardium was again found to produce the dominant echo from the posterior wall (Fig. 7C). The ultrasonic reflections from the pericardium were equal to or slightly greater than those from the posterior wall.
Klein
et al.
A. NORMAL
PWPEP
PERiCARDlAL EFFUSION
Figure 9.
Right venticular (RV) and intrapericardial recorded simultaneoudy. As right (IP) pressures ventricular pressure rises during contraction, the intrapericardial pressure falls. The reduction in intrapericardial pressure correlated with the pericardial motion noted on the “B” presentation as shown in Figure 4.
Pericardial Effusion and Pleural Effusion: During the infusion of saline into the pericardium, leakage developed, as already described. It was noted that the “B” presentation photographs taken during these experiments revealed a relatively echo-free area on both sides of the Leakage from the pericardium (Fig. 8A). pericardium was confirmed by direct visualization of the fluid in the pleural cavity at necropsy. In effect, the pericardium was isolated on both sides by fluid. This finding is considered additional evidence that the pericardium contributes in large part to the dominant echo behind the posterior wall during pericardial effusion. In 1 dog there was total leakage of fluid into the pleural cavity, and autopsy proved that no pericardial effusion existed. Even though pulmonary and posterior wall echoes were separated, this finding was not consistent with pericardial effusion because the dominant echo of the pericardium was absent from its expected position immediately anterior to the echoes arising in the lungs (Fig. 8B). Relation of Intrapericardial Pressure to Motion of the Posterior Wall and Pericardium: When no pericardial effusion exists the pericardial motion is indistinguishable from that of the heart. When the two structures are separated by fluid, each structure has its own identifiable waveform. The waveform of the posterior wall remains the same until the intrapericardial pressure becomes markedly elevated, at which time the amplitude of the waveform may decrease.
L
c. ~R~AR#~~ AND PLEURAL EFFUStONS
PW Pl.E
L
0.
.
Figure
10.
Summary
of all of the findings.
A, normal posterior waI1 (PW) motion in the absence effusion. Th e random dots behind the of pericardial PW are lung (L) echoes. B, in the presence of pericardial effusion (PE) posterior wall and pericardial (P) echoes are separated by an echo-free area.
C, the addition of pleural effusion (P1.E) shows an echo-free area on both sides of the dominant pericardial echoes. D, pleural effusion can be differentiated from pericardial effusion if the dominant waveform of pericardium is not present between PW and lung (L).
THE
AMERICAN
JOURNAL
OF CARDIOLOGY
Reflected
Ultrasound
The pericardium during the infusion of saline is not always without motion. During ventricular contraction the intrapericardial pressure falls, and the pericardium actually moves slightly about 2 mm. in the same direction as the posterior ventricular wall (Fig. 4 and 9). DISCUSSION These experiments lend additional support to the reliability of reflected ultrasound in the diagnosis of perica:rdial effusion. The anatomic separation that develops between the posterior wall and the pericardium with pericardial effusion is diagnosed ultrasonically by observing the characteristic waveforms on both structures recorded by the “13” presentation. The typical waveform of posterior wall motion is identified visually whether or not pericardial effusion exists. The timing of posterior wall motion is accomplished through the use of a simultaneous electrocardiogram. The initial motion of the posterior wall is anterior immediately after the QRS complex on the electrocardiogram. During diastole the wall moves in a posterior direction away from the transducer.5 These experiments have improved our understanding of the reflecting characteristics of cardiac interfaces. The dominance of reflected echoes from an interface in the heart depends on several factors. Reflected ultrasonic energy is determined by a change in the acoustic resistance of a tissue at an interface. Acoustic resistance is defined as the product of tissue density and velocity of sound in the same medium (pV) .6 When the ultrasonic beam passes from blood to endocardium, epicardium to fluid to pericardium (if pericardial effusion exists), reflected energy is returned to the transducer from each of these interfaces. If the structure has a smooth, flat surface located perpendicular to the direction of the ultrasonic beam and exhibits little or no motion it should reflect a maximal amount of ultrasonic energy. In the case of pericardial effusion, the pericardial echoes are dominant, probably because the pericardium is smoother and less curved and remains relatively stationary. Reflected energy arising from the pericardium appears more dominant than that arising from the endocardial surface of the left ventricle. This finding is caused by the changing curvature of the contracting wall in relation to the relative lack of motion of the fluid-filled pericardium. Also, because of its trabeculations, the endocardium VOLUME
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JULY
1968
and Pericardial
Effusion
55
presents an irregular surface to the ultrasonic beam. Motion of the posterior wall tends to scatter ultrasonic energy. The reasons for the lack of dominance of those echoes reflected from the epicardial surface of the posterior wall require further investigation. Additional evidence to support the conclusion that the pericardium is responsible for the dominant waveform during pericardial effusion was gained when fluid escaped from the pericardial sac during the experiment. The pericardium was then noted to be separated from the posterior wall and lung by fluid. The random echoes returned from the lung were distinguishable from those arising in the pericardium. No distinct waveform could be ascribed to the lung echoes.7 Furthermore, we now believe that pericardial effusion may be differentiated clinically from pleural effusion with the aid of these criteria. The absence of pericardial echoes interposed between the waveform of posterior wall and the random echoes of lung enable us to infer the presence of pleural effusion. Pleural effusion without pericardial effusion was subsequently confirmed after the animal was sacrificed (Fig. 10). The pericardium moved no more than 2 mm. during ventricular contraction because the changes in pressure were minimal in ~ the pericardial sac. The simultaneous recording of intrapericardial and right ventricular pressure revealed that intrapericardial pressure dropped during ventricular contraction. The relation between changes in intrapericardial pressure and pericardial motion is now being investigated. These experiments also furnished evidence that measurement of the thickness of the left ventricular posterior wall can be accomplished ultrasonically. Comparing the measurements taken by ultrasound with those made by using a long calibrated needle inserted through the myocardium revealed identical measurements. fhiM.kRY
An experimental evaluation of the ultrasonic technic. for the diagnosis of pericardial effusion revealed the following: 1. The individual waveforms of posterior wall and pericardium could be differentiated after as little as 50 cc. of saline solution was infused into the pericardium. The waveform of the posterior wall could be quickly identified. When pericardial effusion existed the waveform
Klein
56
et al.
of the posterior wall was separated by an echofree area from the waveform of the pericardium. 2. The pericardium is capable of reflecting more ultrasonic energy than the posterior ventricular wall. 3. Pleural effusion can probably be differentiated from pericardial effusion. 4. The major interface of the left ventricular posterior wall is the blood-endocardium interface. The distance from the blood-endocardium to the epicardium-fluid or lung interface is a measure of wall thickness which compares favorably with direct measurements taken at autopsy.
REFERENCES 1. EDLER, I.
Diagnostic use of ultrasound in heart disease. Acta med. scandinav., 308 (Suppl.): 32,
1955. 2. FEIGENBAUM,H., WALDENHAUSEN,J. A. and HYDE,
3.
4.
5.
6.
ACKNOWLEDGMENT
7.
Dr. Klein thanks Dr. Harvey Feigenbaum for permission to visit his laboratory and observe his technic for evaluating pericardial effusion.
DRUGS 29
cardiac
Dqmseallta
32424 Autonomic Drug-
L. P. Ultrasound diagnosis of pericardial effusion. J.A.M.A., 191: 107, 1965. SEGAL, B. L., LIKOFF, W. L. and KINGLSEY, B. Echocardiography: Clinical application in mitral stenosis. J.A.M.A., 195: 161, 1966. EDLER, I., GUSTAFSON, A., KARLEFORS, T. and CHRISTENSSON,B. Ultrasoundcardiography. Acta med. scandinav., 370 (Suppl.): 9, 1961. FEIGENBAU~~, H., ZAKY, A. and WALDHAUSEN,J. A. Use of ultrasound in the diagnosis of pericardial effusion. Ann Int. Med., 65: 443, 1966. KINSLER, L. E. and FREY, A. R. Fundamentals of Acoustics, chap. 8. New York, 1962. John Wiley & sons. JOYNER, C. R., HERMAN, R. J. and REID, J. M. Reflected ultrasound in the detection and localization of pleural effusion. J.A.M.A., 200: 129. 1967.
IN USE 4/68 - 16441
u 5019/l95
pro~anolol mm
. Aftar 10 mg. &WI isoprenallns up to 10 r&liz over 24 hrs. ; After 2nd 5 qg. dose
Malea No. Patients
Dossge:init.l0mg. then 2.5 & 5 me. dosms
no effect except
A. Good recovexy. B. Gradually improved recovered.
i~~prsasll~ 4 ak/min. give1 with little effect. ardioversion performed ulth reversion to sinus rhythm. soprezmline incr. to l5~g/ll&n* with170 *of sodim bicarbonate over nsxt 3 hrs. for presumptive lactic acidos%s.
pigastric pain, & ther bowel movement with
...proprsnolol in small oral doses may cause profound shock and ~reatitis in susceptible hdividuale; and the amount of isoprenaline required to counteract the effect...is far greater than that ususlly used." Taylor, J.A. (Kaiser Found. Hosp., San F'IWIC~SCO,Calif. Q-potenslon after orsl prO~mOl01. Lancet 1: 532-533 (Mar. 9) I368 [Lettsrs to Editor] Prepared by Paul de Haen, Inc. for the drug index card system,
“de Haen Drugs in Use.” THE AMERICANJOURNAL OF CARDIOLOGY