Normal pericardial fluid in the fetus: color and spectral Doppler analysis

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1 Ultrasound Obstet Gynecol 2001; 18: Normal pericardial fluid in the fetus: color and spectral Blackwell ORIGINAL Science, PAPERLtd Doppler analysis S.-J. YOO*, J.-Y. MIN and Y.-H. LEE *Department of Diagnostic Imaging, Hospital for Sick Children, University of Toronto, Toronto, Canada and Department of Radiology, Samsung Cheil Hospital, Sungkyunkwan University School of Medicine, Seoul, Korea KEYWORDS: Doppler, Fetal echocardiography, Pericardial fluid ABSTRACT Objectives To estimate the incidence of sonographic identification of pericardial fluid in normal fetuses and to evaluate the flow pattern of pericardial fluid by using color and spectral Doppler techniques. Methods We evaluated 27 normal fetuses for the presence of pericardial fluid by using gray-scale two-dimensional and M-mode ultrasound, and color and spectral Doppler techniques. Results Pericardial fluid was detected in 52% of cases by twodimensional and M-mode ultrasound and in 81% of cases by color Doppler. The pericardial fluid moved towards the ventricles during systole and towards the atria during diastole. In 9 of 22 fetuses with pericardial fluid identified by color Doppler, spectral waveforms were obtained. The waveforms confirmed the bidirectional flow pattern identified at color Doppler. In six cases there was monophasic systolic and biphasic diastolic flow. In the remaining three cases, the flow was monophasic during both systole and diastole. Conclusions Pericardial fluid can be identified with color Doppler in the majority of normal fetuses. It characteristically shows bidirectional flow as it moves with ventricular systole and diastole. Spectral waveforms can be obtained from the pericardial fluid. The presence of pericardial fluid per se should not be considered as abnormal. Color-coded pericardial fluid should not be mistaken for coronary artery blood flow. INTRODUCTION A small amount of fluid normally exists in the pericardial space. It facilitates friction-free movement of the beating heart within the pericardial sac. It can be visualized as an echo-free rim along the ventricles and atrioventricular junction at both grayscale two-dimensional and M-mode echocardiography 1,2. DeVore and Horenstein described color Doppler identification of pericardial effusion in the fetus 3. According to their study, pericardial fluid was identifiable with real-time gray-scale and color Doppler ultrasound only in the fetuses with pathological effusion. In the 50 control fetuses, they were unable to identify any fluid collection within the pericardial space with either real-time or color Doppler ultrasound. This is in contrast to the study of Dizon-Townson et al. 2 in which pericardial fluid was identifiable in 71% of normal fetuses by using realtime gray-scale and M-mode echocardiography. The aims of this prospective study were to estimate the incidence of sonographic identification of pericardial fluid in normal fetuses and to evaluate the flow pattern of pericardial fluid by using both color and spectral Doppler techniques. MATERIALS AND METHODS We recruited 30 consecutive fetuses in which no abnormality was found at targeted obstetric sonography. We excluded three fetuses from the final study population because adequate postnatal follow-up data could not be obtained. The gestational age at investigation ranged from 19 to 38 weeks (average, 24.7 weeks). All scans were performed by one investigator (S.Y.) with an ATL HDI 3000 ultrasound machine (Advanced Technology Laboratories, Bothell, WA, USA), using a multifrequency (7 4 or MHz) convex transducer. The fetal heart was first evaluated with two-dimensional ultrasound for the presence of pericardial fluid. As the hypoechoic outer layer of the myocardium could be mistaken for pericardial fluid, the anechoic rim was carefully traced to the cardiac apex to find whether it continued through the ventricular septum 4. If the anechoic rim continued through the ventricular septum, it was considered as a hypoechoic layer of the myocardium. The location of the pericardial fluid seen at two-dimensional ultrasound was recorded. The pericardial fluid was evaluated by M-mode in the four-chamber plane in which the ventricular septum was aligned perpendicular to the ultrasound beam axis (Figure 1) 2. The maximum dimension of the fluid shown at M-mode was measured by using a Correspondence: Dr S.-J. Yoo, Department of Diagnostic Imaging, Hospital for Sick Children, University of Toronto, 555 University Avenue, Ontario, Toronto, M5G 1X8, Canada ( shi-joon.yoo@sickkids.on.ca) Received , Revised , Accepted ORIGINAL PAPER

2 Pericardial fluid was identified by two-dimensional ultrasound in 14 fetuses (52%). It was seen all the way around the ventricles and atrioventricular junction in six, along either right or left ventricle in four, along the ventricular apex in three, and at the atrioventricular junction in one. The depth of the pericardial fluid ranged from 0.8 to 2 mm (Figure 1). Color signals were obtained from the pericardial space in 13 of 14 fetuses with visible pericardial fluid at two-dimensional ultrasound (Figure 2a,b). Color signals were also obtained in 9 of 13 fetuses with no identifiable pericardial fluid at twodimensional or M-mode ultrasound. Therefore, pericardial fluid was identifiable by color Doppler in 81% of the whole study population. The optimum velocity setting for color Doppler visualization of pericardial fluid ranged from 14.4 to 44.3 cm/s (19.2 cm/s in 16 cases). Color signals from pericardial fluid, when visible, were towards the ventricular apex during systole and towards the atria during diastole in all cases. Spectral waveforms could be obtained from the pericardial fluid in 9 of 22 fetuses (41%) with visible color signals. The waveforms confirmed the bidirectional flow pattern shown at color Doppler in all cases (Figure 2c). In six of these nine cases, the systolic flow was monophasic and the diastolic flow was biphasic. In the remaining three cases, the flow was monophasic both in systole and in diastole. The peak velocities for systolic and diastolic flows were (average, 22.8) cm/s and (average, 17.4) cm/s, respectively. DISCUSSION Figure 1 M-mode echocardiogram showing pericardial fluid along the left ventricle. The fluid accumulates along the ventricle during the ventricular systolic phase only (arrows). LV, left ventricle; RV, right ventricle. built-in electronic caliper. When M-mode demonstration of the pericardial fluid was not possible, the maximum thickness of the pericardial fluid shown on a gray-scale image was measured. When it exceeded 2 mm, which is the upper limit of the normal value 1,2, we excluded the fetus from the study population. For Doppler evaluation, the ventricular septum was aligned as parallel as possible with the ultrasound beam axis. Color Doppler sensitivity was maximized at the expense of grayscale image quality by selecting a higher priority setting for color Doppler signals. The velocity limits were adjusted until the pericardial fluid was coded with color signals (Figure 2a,b). The pattern of the pericardial fluid movement during the cardiac cycle was evaluated using a cine-loop display. Finally, spectral waveforms were obtained from the color-coded pericardial fluid, and the peak diastolic and systolic velocities were measured after angle correction (Figure 2c). All babies were delivered after weeks of gestation. None showed any signs of cardiovascular abnormalities either at immediate postnatal physical examination or at more than 6 months of age, according to a telephone interview with the parents. RESULTS A small amount of pericardial fluid is commonly seen at fetal ultrasound during the second and third trimesters 1,2. The fluid measuring 2 mm or less in depth at gray-scale twodimensional or M-mode echocardiography is considered nonpathological. DeVore and Horenstein utilized color Doppler for identification of the pericardial fluid in the fetus 3. They demonstrated that color Doppler signals within the pericardial space were opposite in direction to the color Doppler signals within the ventricles. This phasic movement of the pericardial fluid is secondary to the phasic change in the dimension of the pericardial space. During ventricular systole, the pericardial space around the ventricles expands and the pericardial fluid moves into this expanding space. During ventricular diastole, the pericardial space around the ventricles disappears as the pericardial fluid moves away from the field of view. In our study, spectral waveforms as well as color Doppler signals could be obtained from the moving pericardial fluid. In two thirds of the cases with identifiable spectral waveforms, there was monophasic flow during systole and biphasic flow during diastole. The waveforms from the pericardial fluid coincided with the waveforms from the ventricular outlet and inlet, except that the flow was in the opposite direction. This observation supports the concept that the pericardial fluid moves passively within the pericardial sac secondary to the phasic changes in the atrial and ventricular dimensions. One may claim that the Doppler signals we sampled were from the myocardium. It is very unlikely, however, that Doppler signals from the moving myocardium could be sampled by the conventional Doppler technique that we used. To depict myocardial movement, it is necessary to use the Doppler tissue imaging technique, which requires a low velocity limit to measure a velocity of 15 20cm/s, the lowest wall filter settings and minimal optimal gain 4 6. It is noticeable, on the other hand, that the Doppler waveform from the basal myocardium is similar to that from the pericardial fluid except for its lower peak velocities. The similarity between these two waveforms reflects the fact that the pericardial fluid moves within the confined sac of pericardium secondary to the movement of myocardium. Harada et al. assessed the myocardial tissue Ultrasound in Obstetrics and Gynecology 249

3 velocities in normal fetuses and suggested that tissue Doppler imaging can be utilized for quantitative evaluation of systolic and diastolic function of the ventricles as in postnatal echocardiography 6. It might, then, be worthwhile investigating the effect of ventricular function and pericardial compliance on the Doppler waveform of pericardial fluid or effusion. Although the mechanism is not clear, the outer subpericardial layer of the myocardium is less echoic than the inner subendocardial layer 7. Therefore, the anechoic rim of pericardial fluid should be differentiated from this hypoechoic and sometimes anechoic subpericardial myocardium. The hypoechoic outer myocardial layer characteristically continues through the ventricular septum, where it is sandwiched between the two subendocardial echoic myocardial layers. The anechoic sliver of pericardial fluid is seen peripheral to the hypoechoic myocardial layer. When it is difficult to determine whether the hypoechoic or anechoic rim of the normal fetal heart originates from the pericardial fluid or myocardium 7 9, Doppler examination can be utilized for differentiation. The hypoechoic or anechoic rim originating from the myocardium does not demonstrate any Doppler signals, while the rim originating from the pericardial fluid does. A major concern regarding the presence of an abnormal amount of pericardial fluid is the association with other fetal abnormalities including arrhythmias, anomalies, neoplasms, immune and non-immune hydrops, growth restriction, and chromosomal abnormalites 2. In this context, it is also important to note that pericardial fluid is identifiable sonographically in up to 71% of otherwise normal fetuses 1,2 and that isolated pericardial effusion is not usually associated with an adverse outcome 10,11. DeVore and Horenstein considered that the pericardial fluid identifiable with color Doppler is abnormal because they could not identify any color Doppler signals within the pericardial space in any of their 50 control fetuses 3. Based on this observation, they recommended that the reasons for pericardial fluid accumulation should be sought if abnormal pericardial fluid is detected by color Doppler ultrasound. Their result is contradictory to the result of our present study in which pericardial fluid was identified by color Doppler in 81% of normal fetuses. Our study also demonstrated that color Doppler is more sensitive than gray-scale two-dimensional or M-mode ultrasound in depicting pericardial fluid (81% vs. 52%). Therefore, the pericardial fluid seen on color Doppler is not necessarily more suspicious of a pathological condition than that seen at gray-scale or M-mode echocardiography. Figure 2 Doppler echocardiograms showing bidirectional flow pattern of pericardial fluid (a, b). Color Doppler echocardiograms show that the fluid (arrows) moves towards the ventricular apices during systole (a) and towards the atria during diastole (b). The spectral waveform from the pericardial fluid (c) shows monophasic flow towards the cardiac apex during systole (above the baseline) and biphasic flow away from the apex during diastole (below the baseline). The two peaks of the diastolic flow coincide with the e- and a-waves of the blood flow through the atrioventricular valve. LA, left atrium; LV, left ventricle; RA, right atrium; RV, right ventricle. 250 Ultrasound in Obstetrics and Gynecology

4 Figure 3 Color Doppler echocardiograms in systolic (a) and diastolic (b) phases from a fetus with pulmonary atresia and intact ventricular septum. A vessel-like structure with color signals (arrows) is seen along the diaphragmatic surface of the ventricle. The flow is towards the apex in systolic phase (a) and towards the base in diastolic phase (b). We believe that pericardial fluid identified with color Doppler is a normal finding when it does not exceed 2 mm in depth at two-dimensional gray-scale or M-mode echocardiography. On color Doppler, a thin sliver of pericardial fluid is seen as a linear or curvilinear structure along the outer surface of the heart. Therefore, it can be mistaken for a coronary arterial branch. In our earlier experience of a fetus with pulmonary atresia and intact ventricular septum, we identified a tortuous vessel-like structure along the diaphragmatic surface of the heart on color Doppler, and suspected it to be a coronary artery that was dilated because of ventriculocoronary arterial communications (Figure 3). The color Doppler findings of our case were similar to those of Chaoui et al. s case with ventriculocoronary arterial communications 12. In our case, however, postnatal right ventriculography failed to visualize ventriculocoronary arterial communications or dilated arteries. Therefore, we think that we mistook the color-coded pericardial fluid for a dilated coronary artery. By the same token, one should be very cautious when one utilizes visualization of fetal coronary blood flow as an ominous sign of severe uteroplacental insufficiency 13,14. The coronary artery can be differentiated from the pericardial fluid by continuously sweeping the transducer on real-time examination. The coronary arteries are seen only at the expected locations and out of the imaging planes on subtle sweeping of the transducer. The pericardial fluid, on the contrary, is seen not only along the expected courses of the coronary arteries but also in other locations. In summary, pericardial fluid can be identified with color and spectral Doppler, as it moves passively in the pericardial sac with ventricular systole and diastole. The typical spectral waveform from the pericardial fluid consists of biphasic diastolic flow and monophasic systolic flow, which reflects the pattern of blood flow into and from the ventricles. The presence of pericardial fluid per se should not be considered as abnormal when it does not exceed 2 mm in depth at twodimensional or M-mode echocardiography in the absence of other associated abnormalities. Color-coded pericardial fluid should not be mistaken for coronary artery blood flow. REFERENCES 1 Jeanty P, Romero R, Hobbins JC. Fetal pericardial fluid: a normal finding of the second half of gestation. Am J Obstet Gynecol 1984; 149: Dizon-Townson DS, Dildy GA, Clark SL. A prospective evaluation of fetal pericardial fluid in 506 second-trimester low-risk pregnancies. Obstet Gynecol 1997; 90: DeVore GR, Horenstein J. Color Doppler identification of a pericardial effusion in the fetus. Ultrasound Obstet Gynecol 1994; 4: Garcia MJ, Rodgiguez L, Ares M, Griffin BP, Thomas JD, Klein AL. Differentiation of constrictive pericarditis from restrictive cardiomyopathy: assessment of left ventricular diastolic velocities in longitudinal axis by Doppler tissue imaging. J Am Coll Cardiol 1996; 27: Nagueh SF, Middleton KJ, Kopelen HA, Zoghbi WA, Quiñones MA. Doppler tissue imaging: a noninvasive technique for evaluation of left ventricular relaxation and estimation of filling pressures. J Am Coll Cardiol 1997; 30: Harada K, Tsuda A, Orino T, Tanaka T, Takada G. Tissue Doppler imaging in the normal fetus. Int J Cardiol 1999; 71: Brown DL, Cartier MS, Emerson DS, Shanklin DR, Smith WC, Felker RE. The peripheral hypoechoic rim of the fetal heart. J Ultrasound Med 1989; 8: Jeanty P. Hypoechoic rim of fetal heart. [Letter to the Editor] J Ultrasound Med 1991; 10: Brown DL, Emerson DS. Peripheral hypoechoic rim of the fetal heart. [Letter to the Editor] J Ultrasound Med 1991; 10: Yagel S, Hurwitz A. Fetal pericardial fluid. [Letter to the Editor] Am J Obstet Gynecol 1985; 15: Di Salvo DN, Brown DL, Doubilet PM, Benson CB, Frates MC. Clinical significance of isolated fetal pericardial effusion. J Ultrasound Med 1994; 13: Ultrasound in Obstetrics and Gynecology 251

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