Fetal echocardiography VIII. Aortic root dilatat ion-A marker for tetralog y of Fallot Greggory R. DeVore, MD; Bijan Siassi, MD,' and Lawrence D. Platt, MD• Los Angeles and Pasadena, California s of the Tetralogy of Fallot has increased in incidence during the past decade. Although abnormalitie with associated anomalies structural identifies four-chamber screening examination of the fetal heart are not Fallo! of tetralogy with associated anomalies the hypoplasias, valve semilunar and atrioventricular whether determine to designed was study This alone. view r four-chambe the from identifiable as readily for tetralogy aortic root dilatation, commonly observed in the newborn with tetralogy of Fallo!, is a marker e, circumferenc head diameter, biparietal the of Fallo! diagnosed in utero. In 45 normal (control) fetuses of the made were ts measuremen M-mode and measured were length abdominal circumference, and femur fetuses seven from dimension root aortic The dimension. root aortic and dimension outer biventricular when (18, 19, 20, 23, 32, 33, and 34 weeks' gestation) with tetralogy of Fallot was increased in dimension and head diameter, biparietal noncardiac and compared with cardiac (biventricular outer dimension) root imaging abdomen circumferences, and femur length parameters. In conclusion, incorporation of aortic for allows examination screening routine a during heart fetal the of view r four-chambe with the identification of fetuses with tetralogy of Fallot. (AM J OssrET GvNECOL 1988;159:129-36.)
Key words: Echocardio graphy, tetralogy of Fallot, prenatal diagnosis
Tetralogy of Fallot, which occurs in 7% to I 0% of children with congenital heart disease, has increased in incidence during the past decade.' Because its clinical manifestati on during the newborn period can vary from an unsuspecte d anomaly to severe cyanosis with neonatal compromis e, it would be important to identify tetralogy of Fallot in utero for timely neonatal evaluation and care.'· " Recently investigato rs in the United States and Europe have advocated a fetal cardiovascular "screening evaluation" to be performed in all fetuses undergoing ultrasound evaluation: '·" The image that has been suggested is the four-cham ber inflow tract view. Although a number of malformati ons grossly alter the anatomy of the above, the high ventricular septa! defect and underdeve loped pulmonic outflow tract seen with tetralogy of Fallot are subtle and more difficult to detect. However, a dilated aortic root, commonly seen in the newborn with tetralogy of Fallot, could theoreticall y be observed during the "screening examinatio n" of the fetal heart by imaging of the aortic outflow tract.
From the Departments of Obstetrics and Gynecology' and Pediatrics,' University of Southern California School of Medicine, Los Angeles, and the Genetics Institute, Pasadena." Received for publication Apnl 23, 1987; revised December 9, 1987; accepted January 25, 1988. Reprint requests: Greggory R. DeVore, MD, Director of Materna/Fetal Medicine for Intermountain Health Care, 8th Ave. and C St., Salt Lake City, UT 84143.
The purposes of this study are to determine whether aortic root dilatation occurs during the second and third trimesters of pregnancy in fetuses with tetralogy of Fallot and to examine the clinical presentatio n to ascertain associated factors that could affect perinatal manageme nt.
Material and methods Forty-five normal fetuses and seven with tetralogy of Fallot were the basis for the study. Cltrasound examination (General Electric model RT 3000) for all fetuses consisted of assessment of fetal lie followed by measurement of the biparietal diameter, head circumference, abdominal circumfere nce, and femur length. Once the above were completed, the fetal head, thorax, trunk, and extremities were examined for structural malformati ons. 7 Evaluation of the fetal heart consisted of multiple real-time views as well as M-mode measureme nts of the ventricles and aortic root dimension, as previously re12 ported (Figs. I and 2)."· M-Mode measureme nts of the aortic root were compared with noncardiov ascular growth parameters (biparietal diameter, head circumference, abdominal circumfere nce, and femur length) as well as the biventricul ar outer dimension of the heart (epicardium to epicardium ) obtained at the level of the 1 atrioventri cular valves (Figs. I and 2). ' The in utero diagnosis of tetralogy of Fallot was made on the basis of a ventricular septa! defect with an 129
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July 1988 Am .J Obstct Gyncrol
Fig. I. Aortic root dimension. Real-time-directed M-mode demonstrates the M-mode cursor (M) directed through the aortic root (A) at the level of the semilunar valve. M-Mode measurement of the aortic root dimension (ARD) is taken at the point where the aortic valve opens. The arrows identify the aortic root and the bar represents the aortic root dimension.
Fig. 2. M-mode measurement of the bi ventricular outer dimension. By directing the M-mode cursor (M) perpendicular to the interventricular septum at the level of the mitral and tricuspid valves, the
biventricular outer dimension (BVOD) was measured from epicardium to epicanlium (E) and enddiastole (closure of the atrioventricular valves). R, Right ventricle; L, left \'entricle. (From De Vore GR, Horenstein j, Platt LD. A~I j O!ls·1rr GY~ECOI. 1986; 155: 1066-71.)
overriding aorta (Fig. 3), diminished pulmonary outflow tract dimension (Fig. 4), and discontinuity between the interventricular septum and the aortic outflow tract observed in the left-parasternal long-axis view. If cardiovascular malformations were identified, the patient was informed and given the opportunity to consult with a pediatric cardiologist concerning the diagnosis and subsequent long-term treatment and out-
come. All patients were offered a genetic amniocentesis to examine the chromosomal status of the fetus, irrespective of gestational age. After delivery the diagnosis was confirmed by ultrasound, angiography, or autopsy. Results Normal fetuses. Correlation and regression analysis results have been reported for the aortic root dimen-
Fetal echocardiography. VIII. Tetralogy of Fallot
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1 cm
I NORMAL
TETRALOGY OF FALLOT
Fig. 3. Five-chamber aortic outflow tract view. In the normal fetus the aortic outflow tract (A) is confined to the left ventricle. In the fetus with tetralogy of Fallot, a ventricular septa! defect (V) is present and the aortic outflow tract straddles the ventricular septum. These images are from fetuses at 20 weeks' gestation. The stif1pli·d area represents the aortic outflow tract. LV, Left ventricle; RV. right ventricle; LA, left atrium.
sion and the biparietal diameter, head circumference, abdominal circumference, and femur length. 1' The correlation coefficient between the biventricular outer dimension and aortic root dimension was 0.943, with an R" of 0.88 (p < 0.00 I). The line of best fit as determined by regression analysis was: y = mx + b, in which y is the aortic root dimension and x is the biventricular outer diameter. Fig. 5 shows the 95%, 50%, and 5% confidence limits for the biventricular outer dimension and aortic root dimension. Fetuses with tetralogy of Fallot. All fetuses with tetralogy of Fallot demonstrated dilatation of the aortic root dimension when compared with the biventricular outer dimension and uninvolved noncardiovascular organ systems (Figs. 6 and 7). There was no evidence of cardiomegaly (Fig. 8). The following are case summaries for each of the fetuses with tetralogy of Fallot. Second trimester diagnosis Case 1. A 24-year-old woman with class C diabetes with a history of giving birth to two children with congenital heart disease underwent fetal echocardiographic exmaination at .20 weeks' gestation. Real-time views of the heart demonstrated the following abnormalities: a ventricular septa! defect, an overriding aorta, and disproportion between the aortic and pul-
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Fig. 4. Short-axis view of the aortic and pulmonic outflow tracts. The pulmonic (P) and aortic (A) outflow tracts in the normal fetus are of similar size, whereas the pulmonic outflow tract in the fetus with tetralogy of Fallot is diminished in size (arrows). These views are from 20-week-old fetuses. The stippled area represents the pulmonary outflow tract. RA, Right atrium; RV, right ventricle.
monic outflow tract (Figs. 3 and 4). M-Mode measurements of the aortic root demonstrated it to be dilated (Figs. 6 and 7), with a normal biventricular outer dimension (Fig. 8). Measurements of the bi parietal diameter, head circumference, abdominal circumference, and femur length were appropriate for gestational age. Genetic amniocentesis revealed a 46,XX karyotype. The patient elected to continue the pregnancy. Serial measurements of the aortic root dimension showed it to increase at a rate greater than expected (Fig. 9). After repeat cesarean section, a 4550 gm girl with land 5-minute Apgar scores of 9 and 9 was delivered. A neonatal echocardiogram confirmed the in utero diagnosis. The infant was asymptomatic and discharged home with the mother. Case 2. A 21-year-old woman (gravida I) was referred for ultrasound examination at 18 weeks' gestation because of first trimester exposure to penicillin, a recently suggested cardiovascular teratogen. 11 Real-time examination of the fetal heart demonstrated tetralogy of Fallot. M-Mode quantitation revealed an increased aortic root dimension (Figs. 6 and 7) and a normal biventricular outer dimension (Fig. 8). Genetic amniocentesis demonstrated a 46,XY karyotype. After counseling with a pediatric cardiologist, the patient decided not to continue the pregnancy because of the potential financial and emotional liabilities. Prostaglandin in-
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July 1988 Am .J Obstet Gynccol
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BVOD (CM) Fig. 6. Aortic root dimension (ARD) in seven fetuses with tetralogy of Fallot compared with the biventricular outer dimension (BVOD). This demonstrates that the aortic root dimension was dilated in comparison with the biventricular outer dimension, suggesting that the size of the aortic root was out of proportion to the biventricular outer dimension. The number above each square corresponds to the case number in the text.
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Fetal echocardiography. VIII. Tetralogy of Fallo!
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duction of labor occurred at 21 weeks' gestation. Autopsy confirmed the prenatal diagnosis of tetralogy of Fallot. Case 3. A 37-year-old woman (gravida 3, para 2) underwent genetic amniocentesis at 16 weeks' gestation. Increased amniotic fluid ·was noted as well as a "double bubble" within the abdominal cavity. After being in-
formed of the results of the genetic amniocentesis (46,XY), the patient was referred for fetal echocardiography at 19 weeks' gestation. Real-time examination demonstrated tetralogy of Fallot with a dilated aortic root dimension (Figs. 6 and 7) and a normal bi ventricular outer dimension (Fig. 8). After consultation with a pediatric neonatologist and cardiologist, the patient
134 Devore, Siassi, and Platt
July 1988 Am J Obstet Gynecol
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Table I. Malformations of the fetal heart in which the aortic root dimension can be abnormal* Aortic root dimension Malfonnation
Increased
Decreased
Tetralogy of Fallot Coarctation of aorta Truncus arteriosus Hypoplastic left ventricle Hypoplastic left ventricle with transposition
x x
x
x
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*Malformations diagnosed at the Los Angeles County/University of Southern California Women's Hospital in which the aortic root dimension was quantitated as described in this study.
chose not to continue the pregnancy. The pregnancy was interrupted at 21 weeks' gestation by dilatation and extraction. The heart was removed intact and examination confirmed the prenatal diagnosis. Case 4. A 29-year-old woman (gravia 2, para l) was referred for fetal echocardiographic examination at 23 weeks' gestation because of suspected situs inversus. The patient had delivered her first child in another country, with neonatal death occurring secondary to complications from an atrioventricular canal defect. Fetal echocardiographic examination demonstrated tetralogy of Fallot with a dilated aortic root dimension (Figs. 6 and 7) and a normal bi ventricular outer dimension (Fig. 8). The patient declined genetic amniocentesis and underwent termination of pregnancy by
dilatation and extraction. No tissue was available for subsequent evaluation. Third trimester diagnosis Case 5. A 41-year-old woman (gravida 3) was referred at 34 weeks' gestation because of a concern for intrauterine growth retardation. Ultrasound examination demonstrated the following abnormalities: tetralogy of Fallot with a dilated aortic root dimension (Figs. 6 and 7), normal biventricular outer dimension (Fig. 8), microcephaly with ventriculomegaly, enlarged kidneys with cortical hypertrophy, and placenta previa. The patient, who had declined genetic amniocentesis at 16 weeks' gestation, chose not to undergo the procedure because of the certain cesarean section necessitated by the placenta previa. After delivery at 39 weeks' gestation, the above abnormalities were confirmed and a karyotype demonstrated trisomy 18. Neonatal death occurred within 2 weeks of birth. Case 6. An 18-year-old woman (gravida I) was referred for fetal echocardiography because of hydrocephaly and bilateral hydronephrosis noted during a dating examination at 32 weeks' gestation. Hydrocephaly and bilateral hydronephrosis were confirmed. In addition, tetralogy of Fallot with a dilated aortic root dimension (Figs. 6 and 7) and a normal biventricular outer dimension (Fig. 8) were noted. Because of the above anomalies, genetic amniocentesis was suggested; it demonstrated trisomy 18. Given the above information, the patient chose not to undergo surgical intervention should fetal distress occur during labor. Spontaneous labor occurred at 39 weeks' gestation with concomitant fetal distress followed by vaginal delivery
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of a 2780 gm girl with Apgar scores of l (1 minute) and 5 (5 minutes). Neonatal death occurred within 48 hours of birth. Case 7. A 28-year-old woman (gravida 2) was referred at 33 weeks' gestation because of a fixed fetal heart rate of 100 beats/min. Ultrasound examination demonstrated a fetus appropriate in size for 33 weeks with tetralogy of Fallot and a dilated aortic root dimension. The fetal heart rate was consistent with sinus brady11 cardia as assessed with M-mode echocardiogr aphy. and Spontaneous labor occurred at 39 weeks' gestation a 3600 gm male infant with 1- and 5-minute Apgar scores of 8 and 9 was delivered vaginally. At 5 hours of age the newborn became cyanotic. At 8 hours of age cardiac catheterizatio n was performed, which confirmed the in utero diagnosis of tetralogy of Fallot. At 12 hours of age a modified right Blalock-Taus ig anastamosis was performed.
Comment During the past 5 years fetal echocardiogr aphy has taken its place as a valuable diagnostic modality by which major structural and functional abnormalities of the cardiovascula r system can be detected during the second and third trimesters of pregnancy. One of the limitations hindering its wide application, however, is the complexity of the examination for the sonographer not trained in fetal echocardiogr aphy. We recently suggested imaging of the four-chambe r view for each fetus undergoing an ultrasound examination, because the majority of malformation s detected at our center altered the structural integrity of the heart (endocardial cushion defect, large ventricular septal defect) or presented with marked ventricular disproportion (hypoplastic right and left ventricles, coarctation of the 5 aorta)." 5 Recently Allan et al. reported that 80% of heart detected curthe of structural malformation s of abnormalbecause rently in their unit are referred the screenduring noted ities of the four-chambe r view sonografetal cular ing examination by noncardiovas hypoplastic a included phers. The anomalies described left ventricle; mitral, pulmonary, or tricuspid atresia; and a double inlet ventricle; tetralogy of Fallot was not listed. Because the clinical presentation of tetralogy of Fallot in the newborn period can vary, it would be important to identify the afflicted fetus in utero. From our experience the aortic root can be readily imaged in the left-parastern al or five-chamber plane (Fig. 3), and it has the potential for being a marker for congenital heart disease (Table I). In this study seven cases of tetralogy of Fallot were identified in utero and all demonstrate d dilatation of the aortic root when compared with cardiovascula r (biventricula r outer dimension) and noncardiovas cular (biparietal diameter, head circumferenc e, abdominal circumferenc e, femur
Fetal echocardiography. VIII. Tetralogy of Fallo!
135
length) organ systems. Dilatation of the aortic root dimension as ascertained by comparing it with nomograms of the biparietal diameter, head circumferenc e, abdominal circumferenc e, or femur length provides the advantage of using a nonaffected organ system (in the presence of noncardiovas cular malformation s), and it does not require knowledge of gestational age, as is 15 required with previously reported nomograms. Should the aortic root dimension be increased and the examiner be unsure as to whether this is the resuk of a dilated heart, comparing the aortic root dimension with the biventricular outer dimension will enable one to assess aortic root dimension dilatation: In tetralogy of Fallot, the aortic root dimension is out of proportion to the biventricular outer dimension. The clinical management of the fetus with tetralogy of Fallot is dependent on the gestational age at the time of diagnosis. Of the four fetuses diagnosed in the second trimester, three had noncardiovas cular malformations and one did not. The patient in case l chose not to terminate the pregnancy, even though she had given birth previously to two children with congenital heart defects. The reasons for continuing the pregnancy were the absence of ultrasound-d etectable structural malformation s of noncardiovas cular organ systems, a normal karyotype, and a functional pulmonary valve with a pulmonic root dimension 40% the size of the aortic root dimension. In the remaining three patients (cases 2, 3, and 4) major factors for termination of pregnancy were the associated noncardiovas cular anomalies as well as the emotional and financial difficulties perceived from previous experience or counseling with a pediatric cardiologist as to long-term care. Two of three fetuses diagnosed in the third trimester had structural defects of noncardiovas cular organ systems as well as trisomy 18. In both cases the route of delivery was dictated by either obstetric (cesarean section for placenta previa in case 5) or maternal (vaginal delivery for fetal distress in case 6) consideration s. Case 7 illustrates the benefits of fetal diagnosis, in that neonatal care was provided at a tertiary care center in which surgery was performed within 12 hours of birth. In conclusion, examination of the aortic root during a screening examination of the fetal heart will enable the detection of aortic root dilatation. When this is identified, a consultative echocardiogr aphic examination should be performed and the type of anomaly ascertained (Table I). Once done, careful examination of noncardiovas cular organ systems as well as karyotyping should be considered, because the presence of noncardiovascular structural defects occurs in 33% and an abnormal karyotype is found in I 0.5% of newborns 16 with congenital heart disease. After completion of a fetal anomaly profile, care of the patient and fetus can be accomplished in an appropriate manner.
136 DeVore, Siassi, and Platt
REFERENCES I. CDC Sur\'eillance Summaries. Temporal trends in the incidence of malformation in the United States, selected years, 1970-71, 1982-3. MMWR 1985;34: lss-3ss. 2. Rowe RD. Tetralogy of Fallot. In: Keith JD, Rowe RD, Vlad P, eds. Heart disease in infancy and childhood. 3rd ed. New York: Macmillan Publishing Co, 1978: 470-505. 3. Rowe RD, Freedom RM, Mehrizi A, Blood KR. The neonate with congenital heart disease. 2nd ed. Philadelphia: WB Saunders, 1981 :286-300. 4. De Vore GR. The prenatal diagnosis of congenital heart disease: A practical approach for the fetal sonographer. JCC 1985;13:229-45. 5. Allan LO, Crawford DC, Chita SK, Tynan MJ. Prenatal screening for congenital heart disease. Br Med J 1986;292: 1717-719. 6. De Vore GR, Sarti D, Siassi B, Horenstein J, Platt LO. The prenatal diagnosis of cardiovascular malformations in the fetus with situs inversus viscerum during the second trimester of pregnancy. JCU I986;I4:454-7. 7. De Vore GR, Hobbins JC. The diagnosis of structural abnormalities in utero. Clin Perinatol 1979;6:293-3I9. 8. DeVore GR, Siassi B, Platt LD. Fetal echocardiography IV. M-Mode assessment of ventricular size and contractility during the second and third trimesters of pregnancy in the normal fetus. AM J 0BSTET GYNECOL 1984;150: 981-8. 9. DeVore GR, Siassi B, Platt LD. The use of the abdominal circumference as a mean of assessing M-mode ventricular dimensions during the second and third trimesters of pregnancy in the normal fetus. J Ultrasound Med 1985; 4:175-82.
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10. DeVore GR, Siassi B, Platt LO. The use of the femur length as a means of assessing M-mode ventricular dimensions during the second and third trimesters of pregnancy in the normal fetus. JCU 1985; 13:619-25. 11. De Vore GR, Siassi B, Platt LO. The use of the head circumference as a means of assessing M-mode ventricular dimensions during the second and third trimesters of pregnancy in the normal fetus. (in press). 12. De Vore GR, Siassi B, Platt LO. Fetal echocardiography V. M-Mode measurements of the aortic root dimension and aortic valve excursion in the second and third trimester in the normal human fetus. A~t J OBSTET GY:-