Basic technique of fetal echocardiography

Basic Technique of Fetal Echocardiography Charles M. McCurdy Jr and Kathryn L. Reed The fetal heart is the organ system most commonly affected with congenital disease. Though risk factors exist for congenital heart disease (eg, family history, toxin exposure, maternal illness, abnormal karyotype, and other fetal anomalies), the fetal heart is most often examined as part of a routine evaluation of the fetal anatomy in the fetus with no identifiable risk factors. The importance of a systematic, complete assessment of the cardiac axis cannot be overemphasized. All aspects of sonography (ie, real time, M-mode, pulsed, and color Doppler) can provide unique and integral information in evaluating the fetal heart and thorax. Copyright 9 1993 by W.B. Saunders Company

ONG E N I T A L H E A R T disease (CHD) accounts for approximately 25% of all fetal anomalies. Six to 10 neonates per 1,000 liveborns are diagnosed with CHD. 1 This represents roughly six times the incidence of neural tube defects, and more than 10 times the incidence of anomalies affecting any other organ system. The impact of the congenitally abnormal heart is dramatic. More than 50% of childhood deaths are causally related to CHD, and 3% of perinatal losses are secondary to

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CHD.a, 2

Once an abnormal fetal heart has been diagnosed, additional abnormalities should be considered. Roughly one quarter of affected fetuses have other structural anomalies, and 12% to 35% have an abnormal karyotype. Of those fetuses with abnormal chromosomes, 50% to 80% of affected fetuses also have an anomalous heart, although not all can be discovered with ultrasound antenatally (eg, atrial septal defect, ventricular septal defect, and patent ductus arteriosus). 3-s Whereas most cardiac anomalies occur in pregnancies not identified by pre-existing risk factors, clinical risk factors for CHD should lead to a targeted evaluation of the fetal heart. A family history of CHD is the reason for referral for sonography in approximately one third of patients (Table 1). Polygenic inheritance is the rule in CHD and conveys a familial recurrence risk of 3% to 5% overall. Certain lesions, such as hypoplastic left heart, coarctation, and truncus arteriosus, may recur at a rate 2 to 3 times greater than the risk projected with multifactorial inheritance alone; and autosomal dominant syndromes can recur in 50% of offspring. 6 Approximately 50% of recurrent heart lesions are of the same type as the previously diagnosed lesion. 4,7 Maternal risk factors identify another 10% to 15% of at-risk gestations

and include diabetes, isoimmunization, connective tissue disorders, phenylketonuria, and advanced maternal age. 4,s,7,8A history of teratogen exposure (eg, lithium, isotretinoin, rubella virus infection, and alcohol exposure) should be ascertained and targeted cardiac evaluation recommended. 4-7 Finally, a pregnancy complicated by preterm labor, amniotic fluid abnormalities, growth retardation, and other fetal anomalies should be further evaluated with fetal echocardiography. Table 1 includes indications and outcomes of evaluation for a sample group of gravidas. Diagnosis of fetal cardiac abnormalities currently relies on real-time ultrasound. This mode of noninvasive diagnosis has been used since the early 1970s and provides two-dimensional realtime evaluation of fetal anatomy, as well as evaluation of the function of the fetal heart. No other modality, ie, magnetic resonance imaging or computed tomography (CT) scanning, currently offers the clinician this valuable, combined approach to diagnosing fetal abnormalities. The recent use of pulsed Doppler and color Doppler in fetal echocardiography allows the sonographer a means of evaluating the fetal cardiac anatomy and function. Following a brief review of the embryology of the fetal heart and great vessels, this article discusses the common views the sonographer may use to detect a predominance of fetal cardiac lesions on screening evaluation. Additional views of the fetal heart and methods of

From the Division of Maternal-Fetal Medicine, University of Arizona Health Science Center, Tucson, AZ. Address reprint requests to Charles M. McCurdy, Jr, MD, Assistant Professor, Division of Maternal-Fetal Medicine, University of Arizona Health Sciences Center, 1501 N Campbell Ave, Tucson, A Z 85724. Copyright 9 1993 by W.B. Saunders Company 0887-2171/93/1404-0001505. 00/0

Seminars in Ultrasound, CT, and MRI, Vol 14, No 4 (Aug ust), 1993: pp 267-276

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Table 1. Pregnancies Referred for Echocardiography Indication for Referral

Percentage of Total

Percentage Affected

Family history Fetal arrhythmia Noncardiac anomaly Teratogen exposure Diabetes Abnormal referring sonogram Aneuploidy Hydrops

30.3 17.8 11.4 9.9 9.4 3.9 2.7 2.6

1 1.6 23.1 2 3.1 50 25 33.3

(Reprinted with permission. 9)

assessment that can assist in the diagnosis of complex CHD are discussed as well. EMBRYOLOGY Fetal blood and blood vessels begin to form at

approximately 18 days of embryologic life. Intrinsic fetal heart activity begins at approximately 21 days postconception, and the fetal heart tube begins to circulate blood by 26 to 27 days gestational age. Formation of the fetal heart tube results from the migration of angioblastic tissue of mesenchymal origin that aggregates to form paired cardiogenic cords. The heart tube is formed approximately 18 to 19 days postconception. Canalization of the cardiogenic cords results in paired heart tubes that subsequently fuse to form a single chamber. This layer ultimately becomes the endocardium of the mature heart. During the fourth embryologic week, the heart tube convolutes as a function of disproportionately greater growth than the surrounding fetal thorax. Septation begins in the fourth embryologic week with partitioning of the atrioventricular canal and is completed with the formation of the membranous interventricular septum by the seventh week.10,H Initially, three pairs of veins--vitelline, cardinal, and umbilical--drain blood into the developing heart. Of these primordial structures, the left umbilical vein persists in the developed fetus, and portions of the cardinal veins become venous drainage of the upper body. The bulbis cordis is divided into separate channels in the fifth week with formation Of truncal ridges. Subsequent spiral invagination of the truncal ridges separates the bulbis cordis and truncus arteriosus into the aorta and the concentrically spiralling pulmonary artery. Completion of this

process occurs by the seventh embryologic week. 10 SCREENING ULTRASOUND EXAMINATION

Any ultrasound examination should evaluate the pregnancy for the presence or absence of cardiac motion and the localization and biometric dating of the gestation. The presence of abnormalities in the maternal pelvis (eg, adnexal masses, uterine anomalies, free peritoneal fluid) should be assessed, as well as abnormalities in the orientation of the uterus in the pelvis. Localization and evaluation of the placenta and a subjective, or semiquantitative, assessment of amniotic fluid volume should be performed. 12 Following biometric assessment of the fetus, a systematic screening of the fetal anatomy should be undertaken, lz,13 Each fetal organ system should be evaluated in multiple planes with a systematic approach that allows a reproducible and thorough fetal anatomy review. Examination of the fetal thorax and fetal heart for the possibility of anomalies should be performed by a transabdominal approach in all gestations beyond 14 to 16 weeks; and transvaginal imaging may be helpful earlier than 14 weeks in some situations. FETAL ECHOCARDIOGRAPHY Four-Chamber View

After determining the orientation of the fetus within the gravid uterus, the sonographer should evaluate the fetal thorax in multiple planes. The most common screening scanplane used to assess the fetal heart is the "four-chamber view," achieved by assessing the chest serially in transverse planes. Once the fetal heart can be visualized, slight cephalad angulation of the transducer provides the standard four-chamber view. Figure 1 shows the four-chamber view of the fetal heart. The fetal thoracic wall should appear oval, and the fetal heart should be centrally located in the anterior third of the chest. The normal fetal heart occupies approximately 30% to 40% of the area of the fetal chest as seen in the four-chamber view. The inclination of the fetal heart, relative to the midline, is to the fetal left at 35~ to 55 ~. Examination of the internal structures of the fetal heart in this plane reveals four chambers. Atrial chambers and ventricular

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B

RV TV

M

LA

Fig 1. (A) Apical four-chamber view. Ultrasound image with the apex of the fetal heart nearest the transducer. All chambers of the fetal heart are visible. The interatrial and interventricular septa are seen as well as the atrioventricular valves. The foramen ovale (FO) and pulmonary vein(s) (PV) can be seen. LA, left atrium; LV, left ventricle; RV, right ventricle; RA, right atrium. (B) Illustration of apical four-chamber view. MV, mitral valve; TV, tricuspid valve; and SVC, superior vena cava.

chambers are paired and oriented in the chest such that an imaginary line beginning at the thoracic spine and bisecting the chest first enters the left atrium, passes through the atrioventricular septum, and exits the fetal heart through the more anterior right ventricle, which is located in the midline. The interatrial and interventricular septa should be visible on the four-chamber view as well as other cardiac structures, including the foramen ovale, foramen ovale flap, and the atrioventricular valves. The four-chamber view is sensitive for noncardiac thoracic lesions as well as for cardiac lesions. The descending aorta can be seen in

cross-section in the posterior midline of the fetal chest. Other anechoic structures in the posterior chest include the fetal trachea and esophagus in cases where these structures are fluid filled. The lungs should be homogenous in appearance, symmetrical, and slightly more echolucent than the fetal liver. The sonographic appearance of the fetal lungs most closely resembles the appearance of the immature placenta. As gestation progresses the echodensity of the fetal lungs increases; however, attempts to correlate this increased echodensity with pulmonary maturity have little clinical value, a4 The fetal thymus also lies in the superior mediastinum in this plane. Because of its similar echodensity to the fetal lung, however, it is usually not seen on the routine evaluation of the fetal chest. Figure 1 shows the apical four-chamber view obtained by sliding the transducer along a transverse plane of the four-chamber view until the apex of the fetal heart is closest to the transducer. This view is obtained most easily if the fetus is supine within the uterus. Sliding the transducer to the fetal right or left side brings the image of the fetal heart into a transverse alignment and affords the "transverse long-axis four-chamber" view. The value of the transverse long-axis view of the four-chambered fetal heart is improved resolution of the membranous portion of the interventricular septum. Finally, a variant of the four-chamber view, with the apex furthest from the transducer, is obtained when the fetus is prone and the base of the heart is closest to the transducer. The value of the four-chamber view in screening for cardiac abnormalities is well established. This sonographic scan plane alone should detect 60% or more of fetal cardiac anomalies. 9,15-17 Some of the lesions that can be detected with the four-chamber view are included in Table 2.

Views of the Outflow Tracts In addition to the four-chamber view, routine evaluation of the fetal heart should include examination of the great vessels. After obtaining the four-chamber view, the sonographer slides the transducer over the gravid abdomen toward the fetal midline to bring the fetal heart into a transverse plane called the four-chamber

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Table 2. Cardiac Anomalies That Can Be Evaluated with the Four-Chamber View Hypoplasia of ventricles Single ventricle Large septal defects Atrioventricular canal defect Double outlet right ventricle Tetralogy of Fallot Coarctation of aorta Situs Inversus Ectopia cordis Cardiac tumors AV valve atresia and stenosis Ebstein's anomaly Pericardial effusion Premature closure of ductus arteriosus Premature closure of foramen Cardiomyopathy Cardiac hypertrophy Dextrocardia

long-axis view. From this view of the heart, the great vessels can be visualized. The left ventricle outflow tract and ascending aorta are seen with slight angulation of the transducer cephalad from the four-chamber view. In this view the left ventricle, aortic valves, and proximal aorta are clearly identified (Fig 2). In addition, a portion of the pulmonary artery, right ventricle, tricuspid valve, right atrium, and superior vena cava are visible. The pulmonary artery can be evaluated by sliding the transducer cephalad from the scan plane that is used to evaluate the left ventricular outflow tract and aorta. In the latter plane, the right ventricle, pulmonic valve, and pulmonary artery can be evaluated for proper orientation and size. The transverse aorta, ductus arteriosus, tricuspid valve, left pulmonary artery, and portions of pulmonary veins also should be seen (Fig 3). An additional method for examining the fetal outflow tracts is to begin with the apical four-chamber view and then to angle the scan plane cephalad to the "fivechamber" view in which the aortic root appears in a central position in the heart, between the atria (Fig 4). Further angulation captures the right outflow tract which is superior and anterior to the main pulmonary artery. The combination of the four-chamber view with this evaluation of the outflow tracts allows detection of up to 80% of identifiable cardiac lesions. 17Atretic or obstructive lesions of left or right outflow tracts, aorta, or pulmonary artery can result in dilation of the proximal unaffected

or affected ventricle. Hypoplasia of the obstructed ventricle also may develop, depending on the severity and duration of the specific lesion. Conotruncal lesions and transposition can also be detected in the examination of the great vessels. Short-Axis View

The transventricular short-axis view can be obtained by starting with the long-axis fourchamber view and rotating the transducer 90 ~, thus imaging the paired ventricles in short axis. This view allows the examiner to evaluate the symmetry of the ventricles, the presence and location of the papillary muscles, the size and shape of the ventricles, and the relative thickness of the ventricular myocardium and muscular septum (Fig 5). M-mode interrogation in this view can be used to measure fractional shortening and to estimate cardiac work. Movement of

TV"

~

SVC

RA/ Fig 2. (A) Left ventricular outflow tract/long axis. Ultrasound image obtained with mild cephalad angulation of the transducer from the transverse four-chamber view. The left ventricle (LV), aortic valve, and ascending aorta (AO) are highlighted in this view. The right ventricle (RV), right atrium (RA), and pulmonary artery (PA) can be seen also. (B) Illustration of the left ventricular outflow tract/long axis. TV, tricuspid valve; SVC, superior vena cava.

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atrium. The tricuspid valve may be seen between the right ventricle and atrium. The inferior vena cava (IVC) enters the right atrium inferiorly. The short axis/great vessel view may also be used in the assessment of the great vessels (Fig 7). In this view the right ventricle, pulmonary valve, pulmonary artery, and right pulmonary artery are seen in positions analogous to a "doughnut" surrounding the central aortic root at the level of the semilunar valves. This view may not be intuitively obvious to the inexperienced echocardiographer. If the fetus is right thorax anterior, a lower thorax transverse plane

Fig 3. (A) Right ventricular outflow tract/long axis. Sliding of the transducer cephalad from the LV outflow tract view should reveal the right outflow tract. In this view the right ventricle (RV), pulmonic valve (PV), and proximal pulmonary artery (PA) are seen. The aorta (AO) and superior vena cava (SVC) may also be seen. (B) Illustration of the right ventricular outflow tract/long axis. TV, tricuspid valve.

the transducer in the cephalic direction allows evaluation of the membranous interventricular septum as well as the tricuspid (anterior) and mitral (posterior) valves. Great Vessel Views

The great vessels may be assessed in the long axis of the fetus with the long axis/great vessel view, which is accomplished from the anterior fetal thorax (Fig 6). Rotating the transducer 90~ from the apical four-chamber view allows visualization of the great vessels as they exit the fetal heart. The right ventricle is most anterior. Superiorly, from anterior to posterior, the proximal pulmonary artery and pulmonic valve are seen, then the aorta, and finally the most posterior, superior structure, the superior vena cava (SVC), which is seen as it enters the right

Fig 4. (A) Five-chamber view. Cephalad angulation of the ultrasound transducer from the apical four-chamber view reveals the root of the aorta (AO) exiting the left ventricle (LV} in a central position between the right and left atria (RA and LA). The aortic valve should be visible. (B) Illustration of the five-chamber view. RV, right ventricle; TV, tricuspid valve; MV, mitral valve.

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right ventricle is the most distal structure imaged. Two-dimensional evaluation of the great vessels can be continued with the imaging of the ductal and aortic arches. The ductal arch can best be viewed longitudinally with the fetus supine in the uterus. The ductal arch view consists of the right ventricle, pulmonary artery, ductus arteriosus, and descending aorta. The appearance of the ductal arch has been likened to a "hockey stick," because it is flattened and lower in the thorax than the aortic arch. The aortic arch can be visualized best from both anterior and posterior approaches in a longitudinal plane to the left of the fetal spine. The "candy cane" appearance of the aortic arch

RV

Fig 5. (A) Transventricular view. This short-axis view of the right and left ventricles (RV and LV) can be imaged with a 90 ~ rotation of the transducer from the transverse four-chamber view. (B) Illustration of transventricular view. The papillary muscles (PM) within each ventricle are shown and should be visible with ultrasound.

through the fetal liver sharply angled obliquely first images the right ventricle, right atrium, and the tricuspid valve; subsequently it views the aortic valve and, finally, the main pulmonary artery and right pulmonary artery. The ductus arteriosus can be seen arching inferiorly and to the left of the fetal heart. In the fetus with the left thorax anterior, angling obliquely down from a posterior thorax origin through the fetal liver approximately between the clavicle and scapula attains a similar image. The ductus arteriosus is most proximal in the image, superior and to the right of the fetal heart, and the

Fig 6. (A) Long axis/great vessel view. This view of the great vessels within the fetal thorax is best imaged with the fetus in a supine position within the uterus. A longitudinal scanplane images (from anterior to posterior) the pulmonary artery (PA), aorta (AO), and superior vena cava (SVC). Aortic and pulmonic valves (AV and PV) are shown as well. The inferior vena cava (IVC) can be seen draining into the right atrium (RA) inferiorly. TV, tricuspid valve. (B) Illustration of long axis/great vessel view. RV, right ventricle,

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alies best evaluated with the short- or long-axis views of the great vessels, or of the ductal and aortic arches. In addition to the anatomy described previously, the normal anatomy of the pulmonary veins, IVC, and SVC are also important. As seen in the long-axis/great vessel view, the SVC and IVC enter the right atrium from superior and inferior positions, respectively. The pulmonary veins, best imaged in the fourchamber view, are seen entering the posterior left atrium. This normal finding may be used to rule out anomalous venous return.

M-Mode Echocardiography

O

Fig 7. (A) Short axis/great vessel view. This imaging plane creates a "doughnut" appearance of the right heart and outflow tract around the central aorta (AO]. In this ultrasound view, the right ventricle (RV), tricuspid valve (TV), and right atrium are anterior. The pulmonic valve (PV), main pulmonary artery, left pulmonary artery (LPA), and right pulmonary artery (RPA) can be seen. The ductus arteriosus (DA) can be seen as it courses toward the descending aorta (Desc AO). (B) Illustration of short axis/great vessel view,

is comprised of the ascending, transverse, and descending aorta. The transverse aorta "wraps" superiorly to the right pulmonary artery. Cerebral vessels arising from the cephalic portion of the aortic arch provide important landmarks that distinguish this arch from the ductal arch. Figure 8 shows the respective arches and adjacent structures. Table 3 lists fetal cardiac anom-

M-mode echocardiography (abbreviated from TM, or "time-motion mode") allows a linear visual image of movement of insonated objects over time. Historically, M-mode scanning has been used to detect fetal cardiac activity. 18 Although still suitable for this purpose, Mmode echocardiography is now used primarily for evaluating fetal arrhythmias, assessing fetal valvular and ventricular size and function, and detecting pericardial effusions. Information about volume flow and ventricular work can be obtained with the addition of Doppler velocity flow information to measurements of valvular and ventricular chamber or wall thickness. Mmode echocardiography is not used in the major•ty of fetal cardiac evaluations, but it can provide unique information about the function and anatomy of the fetal heart in which structural or physiological abnormalities are suspected. M-mode scanning is used primarily for discerning the type of arrhythmia in the affected fetus. Placement of the M-mode cursor over an atrium, atrioventricular valve, and ventricle within the same plane allows inference of a specific conduction defect by the abnormal timing in ventricular or atrial wall movement (Fig 9). The linear observation of valvular movement also provides further indirect evidence of an abnormal conduction system.19,2~

Doppler Echocardiography Doppler echocardiography can be used to assess blood velocity through vessels, heart chambers, and valves. Blood flow volume can be calculated from Doppler velocity measurements with the addition of two-dimensional measure-

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Fig 8. Ductal and aortic arches. These paired sonograms show the different appearance of the ductal and aortic arches. The ductal arch has a flattened, "hockey stick" appearance as the main pulmonary artery exits the right ventricle and ends in the ductus arteriosus, which terminates in the descending aorta (desc AO). The rounded, "candy cane" appearance, as well as the appearance of cephalic vessels (CV) branching superiorly allow rapid identification of the aortic arch to the right in this figure. LA, left atrium; AO, proximal aorta; RA, right atrium.

ment of vessel or valve areas. Changes in flow velocity may be used to detect abnormal cardiac function. 19,21Arrhythmias can be evaluated using the pulsed Doppler method with interrogation of the diastolic and systolic wave forms across atrioventricular valves, and more recently with assessment of Doppler velocity flow patterns in the IVC. 22,23Subtle defects in structure (stenotic or abnormal atrioventricular valves) can be detected with variations from normal expected flow patterns. 3 The addition of color Doppler interrogation to the echocardiographer's evaluation has furTable 3. Cardiac Anomalies That Can Best Be Evaluated With the Great Vessel Views (Short and Long Axis) and Great Vessel Arch Views

Transposition of the great vessels Pulmonary valve stenosis Pulmonary valve atresia Pulmonary valve insufficiency Premature closure of the ductus arteriosus Tetralogy of Fallot Truncus arteriosus Aortic valve stenosis Aortic valve atresia Aortic valve insufficiency Coarctation of the aorta

ther assisted in diagnosing abnormalities of function and structure. Small septal defects may remain undetected until abnormal "jets" of flow are seen with color Doppler. Abnormal turbulence can be detected by this method as well. One primary value of color Doppler is quick identification of suspicious flow patterns that can be interrogated with pulse Doppler. This last utility significantly reduces the time needed to evaluate fetases with suspected C H D . 24 EXTENT OF EXAMINATION

The fetal heart is examined most frequently in the patient without identifiable risk factors as part of an evaluation of the fetal anatomy during a routine ultrasound evaluation. The importance of systematic, complete assessment of the fetal heart cannot be overemphasized. Recognition of the normal cardiac and thoracic anatomy is the basis from which the sonographer identifies abnormal anatomy or function. If an abnormal fetal heart is identified, the remaining fetal anatomy should be assessed carefully for additional abnormalities. In addition, identification of any fetal anomaly should prompt the sonographer to target the fetal heart

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Fig 9. Two-dimensional/Mmode duplex image. In this sonographic image, the two-dimensional image (left) guides the placement of the cursor over an atrial wall, interventricular septurn (IVS), and ventricular wall for M-mode interrogation of cardiac function. The corresponding M-mode image is shown to the right with a synchronous-appearing atrial and ventricular wall motion. Note the premature atrial contraction.

for extensive evaluation. Pregnancies with an abnormal ultrasound evaluation or pregnancies at risk for fetal cardiac anomalies should undergo a targeted evaluation of the fetal heart by

an experienced consultant. This evaluation uses the combination of two-dimensional, M-mode, and Doppler echocardiography to best evaluate the cardiac anatomy and function.

REFERENCES 1. Hoffman JIE, Christianson R: Congenital heart disease in a cohort of 19,502 births with long-term follow-up. Am J Cardiol 42:641-647, 1978 2. Hung J, Ng H, Shei K, et al: Using ultrasonic measurement of cardiac size in predicting congenital heart defect. Fetal Diagn Ther 6:65-73, 1991 3. Reed KL, Anderson CF, Shenker L: Fetal Echocardiography: An Atlas. New York, NY, Wiley/Liss, 1988 4. Reed KL, Sahn D J: A proposal for referral patterns for fetal cardiac studies. Semin Ultrasound CT MRI 5:249252, 1984 5. Copel JA, Cullen M, Kleinman CS: Congenital heart disease and extracardiac anomalies: Associations and indications for fetal cardiac studies. Am J Obstet Gynecol 154:1121-1132, 1986 6. Nora JJ, Nora All: The evolution of specific genetic and environmental counselling in congenital heart diseases. Circulation 57:205-213, 1978 7. Reed KL: Fetal echocardiography. Semin Ultrasound CT MR 12:2-10, 1991 8. Smith DW: Recognizable Patterns of Human Malformation (ed 3). Philadelphia, PA, Saunders, 1982 9. Copel JA, Pilu G, Green J, et al: Fetal echocardiographic screening for congenital heart disease: The fourchamber view. Am J Obstet Gynecol 157:648-655, 1987 10. Moore KL: The cardiovascular system, in (ed): The Developing Human. Clinically Oriented Embryology (ed 4). Philadelphia, PA, Saunders, 1988, pp 286-333 11. Bressler RS: Embryology of the heart, in Elkayam U,

Gleicher N (eds): Cardiac Problems in Pregnancy. New York, NY, Liss, 1982, pp 317-335 12. Leopold GR: Antepartum obstetrical ultrasound examination guidelines. J Reprod Med 5:241-242, 1986 (editorial) 13. The American College of Obstetricians and Gynecologists: ACOG Technical Bulletin No. 116, Ultrasound in Pregnancy. Washington, DC, 1988 14. Cayea PD, Grant DC, Doubilet PM, et al: Prediction of fetal lung maturity: Inaccuracy of study using conventional ultrasound instruments. Radiology 155:473-475, 1985 15. Allan LD, Crawford DC, Chita SK, et al: Prenatal screening for congenital heart disease. Br Med J 292:17171719, 1986 16. Hegge FN, Lees MH, Watson PT: Utility of a screening examination of the fetal cardiac position and four chambers during obstetric sonography. J Reprod Med 32:353-358, 1987 17. Kirk JS, Riggs TW, Comstock CH, et al: The prospective evaluation of fetal cardiac anatomy: A comparison of 4 and 5 chamber views in 5,967 patients. Am J Obstet Gynecol 168:291, 1993 (abstr) 18. Shenker L, Astle C, Reed K, et al: Embryonic heart rates before the seventh week of pregnancy. J Reprod Med 31:333-335, 1986 19. Reed KL: Fetal arrhythmias: Etiology, diagnosis, pathophysiology, and treatment. Semin Perinatol 13:294304, 1989 20. DeVore GR, Siassi B, Platt LD: Fetal echocardiogra-

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phy. III. The diagnosis of cardiac arrhythmias using realtime-directed M-mode ultrasonography. Am J Obstet Gynecol 146:792-799, 1983 21. Silverman NH, Kleinman CS, Rudolph AM, et al: Fetal atrioventricular valve insufficiency associated with nonimmune hydrops: A two-dimensional ecbocardiographic and pulsed Doppler ultrasound study. Circulation 72:825-832, 1985 22. Reed KL, Sahn D J, Marx GR, et al: Cardiac Doppler

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flows during fetal arrhythmias: Physiologic consequences. Obstet Gynecol 70:1-6, 1987 23. Reed KL, Appleton CP, Anderson CF, et al: Doppler studies of vena cava flows in human fetuses: Insight into normal and abnormal cardiac physiology. Circulation 81:498505, 1990 24. Copel JA, Morotti R, Hobbins JC, et al: The antenatal diagnosis of congenital heart disease using fetal echocardiography: Is color flow mapping necessary? Obstet Gynecol 78:1-8, 1991