Diagnosis of fetal ductus arteriosus aneurysm: importance of the three-vessel view
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1 Ultrasound Obstet Gynecol 2005; 26: Published online in Wiley InterScience ( DOI: /uog.1927 Diagnosis of fetal ductus arteriosus aneurysm: importance of the three-vessel view C. M. JACKSON*, G. G. S. SANDOR*, K. LIM, W. J. DUNCAN* and J. E. POTTS* *Division of Cardiology, Department of Paediatrics, and Division of Perinatology, Department of Obstetrics and Gynecology, Children s and Women s Health Centre of British Columbia and The University of British Columbia, Vancouver, B.C., Canada KEYWORDS: aneurysm; ductus arteriosus; three-vessel view ABSTRACT Objective To present four cases of ductus arteriosus aneurysm (DAA) detected by fetal echocardiography and highlight the value of the three-vessel view in the diagnosis of DAA. Methods In addition to the standard fetal echocardiographic views, we examined the three-vessel view in four cases of DAA. The three-vessel view was achieved by sliding the transducer cranially from the four-chamber plane toward the fetal upper mediastinum to demonstrate cross-sections of the main pulmonary artery, the ascending aorta and superior vena cava arranged in a straight line from the left anterior to the right posterior aspect of the mediastinum. DAA was diagnosed when there was a tortuous ductus arteriosus with a dilation that protruded leftward of the aortic arch. Case series In the first case, an insulin-dependent diabetic woman underwent fetal ultrasound examination at 36 weeks gestation showing right-to-left cardiac disproportion and bidirectional flow in the aorta and main pulmonary artery (PA). The three-vessel view showed a dilated ductus arteriosus (DA) which was stenosed at its distal end. In the second case, a woman had fetal ultrasound scans at 38 and 39 weeks gestation for suspected intrauterine growth restriction and oligohydramnios. The scans identified an abnormal aortic arch and the three-vessel view showed an elongated vascular structure at the distal end of the PA, which was the DAA. In the third case, a woman with a high-risk obstetric history had multiple scans showing an abnormal PA to aorta relationship, with an apparent kink in the PA. The three-vessel view clarified that this was the DAA. In the fourth case, a woman was scanned because of a 3-kg weight gain in 1 week. The fetal ultrasound scan showed moderate polyhydramnios with normal fetal growth and normal intracardiac anatomy and flow, and the threevessel view demonstrated a large DA. In each of these cases, the DAA appeared to have occurred in isolation with non-specific clinical findings. Conclusion We advocate the use of the three-vessel view, in conjunction with the standard echocardiography views currently employed, to assist in the diagnosis of DAA. Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd. INTRODUCTION Until recently, ductus arteriosus aneurysm (DAA) was considered to be rare and the etiology thought to be either spontaneous or acquired as a complication of surgical closure of a patent ductus arteriosus (PDA) or after ductal infection 1. Lund et al. cite a 31% complication rate in their earlier review of 65 cases of DAA previously diagnosed in children under 2 months of age, although it is rarely fatal 2. Significant complications include thromboembolism, compression of adjacent structures, infection secondary to bronchial obstruction, left pulmonary artery stenosis and spontaneous rupture 1,3,4. More recently, reports have suggested that DAA may be more common than previously thought, and may be as high as 8.8% as reported by Jan et al. in 2002 in a report of fetal echocardiography of diabetic pregnancies 1. Although imaging of the ductus arteriosus (DA) by ultrasonography has been possible for many years, it is only since 1995 that DAA has been reported using fetal echocardiography. In 1995, Puder et al. described the first case of DAA detected in utero, at 39 weeks gestation 5.Inthe same year, Mielke et al. reported a case of an abnormally S-shaped kinking of the ductus arteriosus with increased systolic and diastolic Doppler flow velocities 6. Correspondence to: Dr G. G. S. Sandor, Division of Cardiology, Children s and Women s Health Centre, 4480 Oak St., Room 1F27, Vancouver, BC, Canada, V6H 3V4 ( gsandor@cw.bc.ca) Accepted: 8 April 2005 Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER
2 58 Jackson et al. There developed a controversy regarding the degree of bend or S-shaped kinking permitted in the normal ductus, which prompted an Opinion by Brezinka in the same journal 7,8. Since that time, several other authors have detected DAA in utero using ultrasonography 3,4,9. The four-chamber and short-axis views have been established for routine screening of congenital heart disease, and local and national protocols for detailed examination of the fetal heart have been created 3. In 1997 Yoo et al. advocated using the three-vessel view in addition to the standard four-chamber view in routine screening in order to increase the detection rate of congenital malformations 10.Toemphasizetheusefulness of the three-vessel view as an easy means of detecting abnormalities involving the ventricular outflow tracts and great arteries, these authors listed a number of cardiac malformations involving both left- and rightsided cardiac malformations in which this view was found to be abnormal. However, no mention was made of the ability to detect a DAA using this view. Since the original description of the three-vessel view, there have been other reports confirming its usefulness and expanding its diagnostic role in fetal echocardiography. With slight angulation of the transducer more anatomical details are demonstrated, including the transverse aorta, ductus, superior vena cava and trachea in the three vessels and trachea view We present reports of four cases of ductus arteriosus aneurysm detected by fetal echocardiography between July 2000 and June 2002, highlighting the value of the three-vessel view as an aid in the diagnosis of DAA, and advocate its use in conjunction with the standard fetal echocardiographic views currently employed. To the best of our knowledge, this method has not previously been described in the diagnosis of DAA. METHODS In addition to the standard fetal echocardiographic views, i.e. the four-chamber, short-axis, left outflow and arch views, three-vessel views were performed during routine examination by our fetal echocardiographic service, which is located in the only tertiary care center for the Province of British Columbia, which has a population of 3.9 million. The three-vessel view is a transverse view of the fetal upper mediastinum and allows abnormal size and abnormal spatial relationships of the arterial trunks to be seen 3.As originally described, this view was achieved by sliding the transducer cranially from the four-chamber plane toward the fetal upper mediastinum. It demonstrates round crosssections of the main pulmonary artery, the ascending aorta and superior vena cava arranged in a straight line from the left anterior to the right posterior aspect of the mediastinum, with a decreasing order of their diameters. By sweeping and manipulating the transducer, it is possible to visualize the right and left pulmonary arteries and the ductus arteriosus sweeping posteriorly to the descending aorta and, by sweeping slightly more cephalad, the transverse aortic arch, which also connects with the descending aorta from a more rightward position than the ductus arteriosus. We used the criteria that Dyamenahalli et al. specified to make a diagnosis of DAA, that is, the presence of a tortuous ductus arteriosus with a fusiform or saccular dilation that protruded leftward of the aortic arch 9. The diameter of the dilated portion of the ductus arteriosus had to be more than the 95th percentile of the normal cross-sectional diameter for gestational age, as described by Tan et al 15. CASE SERIES Case 1 An ultrasound scan at 36 weeks gestation in a 32-yearold insulin-dependent diabetic woman, gravida 3, para 1, documented a larger right side of the fetal heart when compared to the left. Fetal echocardiography at 37 weeks gestation confirmed right-to-left disproportion. Color and pulsed wave Doppler of the descending aorta demonstrated turbulent flow, with evidence of flow reversal. Bi-directional flow was also noted on imaging of the main pulmonary artery (MPA). Imaging of the DA showed slight narrowing of the vessel with dilatation in the distal segment, which appeared to be kinked. The three-vessel view clearly illustrated this (Figure 1a). Doppler interrogation also demonstrated accelerated flow with a peak velocity of 2.0 m/s within the DA at the juxtaductal region (Figure 1b). This was thought to be either a coarctation of the aorta, premature closure of the DA, or a DAA. No other structural or functional anomalies were noted. At 38 weeks gestation, spontaneous vaginal delivery (SVD) resulted in the birth of a 3765-g girl. Mild dysmorphism with increased nuchal skin thickness and retrognathia were noted. The transcutaneous oxygen saturation was 98% in air. She had a soft grade 2/6 early systolic murmur at the upper left sternal edge. A transthoracic echocardiogram performed on day 1 showed a large right ventricle and MPA, the foramen ovale bulging to the right atrium, a narrow, tortuous PDA with a horizontally directed left-to-right shunt on color Doppler and a normal aortic arch. The patient was clinically well and was discharged. Case 2 Fetal echocardiography was performed at 39 weeks gestation on a 21-year-old woman, gravida 1, para 0, after an abnormal aortic arch was detected on a short-axis view of the heart on an earlier scan at 38 weeks performed for intrauterine growth restriction and oligohydramnios. Fetal echocardiography at 39 weeks gestation showed an elongated vascular structure at the distal end of the pulmonary artery connecting with the descending aorta (Figure 2a). Utilizing the three-vessel view, a dilated right-angled DAA was diagnosed (Figure 2b). No other cardiac structural or functional abnormalities were apparent.
3 Ductus arteriosus aneurysm 59 Figure 1 Case 1: (a) Three-vessel view showing the aneurysmal ductus arteriosus (DA). (b) Pulsed Doppler in the distal DA showing increased velocity. Ao, aorta; Desc Ao, descending aorta; SVC, superior vena cava. A 2565-g boy was born by SVD at 40 weeks gestation. Examination was unremarkable. Transthoracic echocardiographic examination, performed within minutes of birth, found a fetal-sized DA with an aneurysm at the aortic insertion point, which enveloped the upper portion of the descending aorta. Bidirectional shunting of blood through the PDA was demonstrated using color flow and pulsed Doppler. Cardiac anatomy and function were otherwise normal. Subsequent echocardiograms over the next month showed uncomplicated closure of the DAA. Case 3 A 34-year-old woman with systemic lupus erythematosus (SLE), gravida 4, para 0, had 4-weekly scans from 25 weeks gestation. Ultrasound scanning at 35 weeks gestation suggested an abnormal pulmonary artery to aorta relationship, with an apparent kink in the pulmonary artery. Fetal echocardiography, performed at 37 weeks gestation, illustrated normal intracardiac anatomy and Doppler flows. Sweeping from the fourchamber view to obtain the three-vessel view, the Figure 2 Case 2: (a) Sagittal view showing color Doppler in a tortuous ductus arteriosus aneurysm (DAA), some of which is out of plane with no color flow visible. (b) Three-vessel view at the level of the ductus arteriosus, showing the DAA, which is clearly not a straight structure as it appears to make almost a right angle. Desc Ao, descending aorta; MPA, main pulmonary artery; PA, pulmonary artery; SVC, superior vena cava. pulmonary arteries were clearly demonstrated and further cephalad the ductal view showed the DAA (Figures 3a and 3b). A 3380-g male baby was born by SVD at 40 weeks gestation. Examination was normal. An echocardiogram performed at 1 day postnatally reconfirmed the DAA. A small residual left-to-right shunt through a horizontal ductus was noted, but imaging was otherwise normal. Subsequent echocardiograms showed uncomplicated closure of the DAA over the next 3 days. Case 4 A 23-year-old, gravida 1, para 0, woman was scanned at 38 weeks gestation because of a 3-kg weight gain in 1 week. Detailed ultrasound examination showed moderate polyhydramnios with normal fetal growth. The cardiac views were difficult, but as the four-chamber view
4 60 Jackson et al. Figure 3 Case 3: (a) Three-vessel view at the level of the ductus arteriosus (DA), showing a rounded lateral protrusion of the DA. (b) The same view as (a) with color Doppler showing turbulent flow. Ao, aorta; SVC, superior vena cava. was abnormal, fetal echocardiography was performed at 39 weeks gestation. Normal intracardiac anatomy and Doppler flow were demonstrated. However, the DA appeared large on the three-vessel view, measuring approximately 9 mm in diameter (Figure 4a and 4b). For comparison, the transverse aortic arch was noted to be 7 mm (within the normal range). Normal flow was demonstrated within the DA. A 3860-g baby boy was born by Cesarean section at 40 weeks gestation. Clinical examination was normal. An echocardiogram was performed at 3 days of age, which showed a PDA with a particularly tortuous course, and a restrictive pulmonary artery end was noted with partial involution of the aneurysmal DA. Flow was left to right. No other cardiac abnormalities were detected. DISCUSSION The exact mechanism by which spontaneous DAA forms in utero remains uncertain, though several theories concerning its pathogenesis have been postulated: Figure 4 Case 4: (a) Three-vessel view of a slightly dilated ductus arteriosus (DA). (b) Same view as in (a) with color Doppler showing mild dilation of the DA and mild turbulence indicating a higher velocity than the transverse aorta or turbulent flow. Ao Arch, aortic arch; Desc Ao, descending aorta; MPA, main pulmonary artery; SVC, superior vena cava. (1) congenital wall weakness resulting from necrosis and mucoid degeneration of the media in the DA 2 ; (2) increased flow through the DA in utero 16 ; (3) intrauterine ductal constriction at its pulmonary artery end, with post-stenotic dilatation of the DA during fetal life 17 ; and (4) abnormal intimal cushion formation or defective elastin in the DA 9. None of these theories can explain DAA formation in all patients. In fact, Jan et al. suggested that given their high observed incidence of DAA in full-term neonates, DAA may in fact be a normal variant of an elongated ductal bump and part of a normal process of spontaneous ductal closure 1. This would, however,implyahighrateofductalclosurein utero.whether or not the DA is a separate pathological entity remains controversial. Not only is the cause of DAA unknown but the incidence is also not known. All the reports may be criticized for ascertainment bias. A controlled study where every woman was scanned at regular intervals throughout pregnancy would be required to be certain of the real
5 Ductus arteriosus aneurysm 61 incidence of DAA. Three of the four cases of DAA described above were found in male fetuses, reflecting the male predominance observed in previous studies of DAA 1. Suggestions that DAA is likely to develop in late gestation are supported by this study, in which no signs of DAA were noted prior to 35 weeks gestation. In Case 1, the DAA was discovered when searching for a cause for the abnormally dilated right cardiac chambers as found by Acherman et al 17.Ineachoftheircases,color Doppler interrogation revealed aneurysmal dilatation of the PDA with turbulent flow along a right-to-left shunt. It may be suggested, therefore, that further investigation of disproportionate left-to-right sided chambers should routinely include visualization of the DA, including the three-vessel view in addition to the more standard views. Since only one of the four cases reported here showed evidence of right sided cardiac enlargement, it is not possible to state whether the DAA reflects or causes abnormal fetal hemodynamics. Case 1 with the marked kink and Doppler acceleration is worthy of comment. The DAA may have been kinked sufficiently to cause stenosis distally resulting in the high velocity. In view of the near equal pressures in the ductus and the aorta, the only other explanation could be that the arterial properties were stiffer causing an apparent stenosis. In Case 2, the DAA was discovered when undertaking more detailed examination after a previous ultrasound examination at 38 weeks gestation suggested an abnormality of the aortic arch. This was also the indication for more detailed scanning in six out of a total of nine fetuses in the paper by Dyamenahalli et al 9. The mother of the baby in Case 1 was known to be an insulin-dependent diabetic. Jan et al. have documented that mothers with poorly controlled gestational diabetes mellitus had a higher than average incidence of neonates with DAA, but only when associated with a large-forgestational age newborn 1. The baby in Case 1 was born at 38 weeks gestation and had a birth weight of 3765 g, which would not indicate poor diabetic control. Dyamenahalli et al. also noted that the mother of one of nine fetuses in their study diagnosed with DAA had diabetes, though no comment was made with regard to whether this was gestational diabetes, or on the degree of control 9. Acherman et al. also comment that four out of 11 of the DAAs they detected were in insulin-dependent diabetics 17. Lund et al. describe similar findings 2. Several of these reports reflect the incidental finding of a DAA in fetuses of diabetic mothers who were undergoing routine echocardiographic evaluation. As diabetic mothers tend to have more ultrasound scans than do mothers with normal pregnancies, it is not clear whether there is an actual association between fetal DAA and maternal diabetes. It is also interesting to note that the mother in Case 2 was known to have blood group A. An association between DAA of the fetus and maternal blood group A has been previously described. Jan et al. found that 47.9% of neonates with DAA had maternal blood group A, as compared with only 29.2% of mothers of neonates without DAA 1. Whether or not this blood group is associated with, or actually predisposes a fetus to, DAA or reflects the proportion of that blood group in that community is not known. The postnatal clinical findings were non-specific. Only one child had a soft, early systolic murmur at the upper left sternal edge, while another had a slightly hyperdynamic precordium which settled within one day of birth, suggesting that clinical examination would not have raised any suspicion of congenital heart disease which might have led to investigation. In Case 1, dysmorphic features were noted; this has also been reported in association with DAA. After birth, detailed echocardiographic examination confirmed the diagnosis of DAA in all four cases, and the ductus was best visualized from the high parasternal or suprasternal short-axis view, where two-dimensional, pulsed and color Doppler demonstrated the abnormal, horizontal course of the DAA. The resolution of the DAA and uncomplicated closure of the PDA was documented in each case. Some reports have commented on observing thrombus formation as being part of the mechanism of resolution of the PDA and DAA, but none of these neonates displayed thrombus extension from the DAA 1,4,9. In summary, echocardiography is an invaluable imaging modality in the detection, evaluation and follow-up of fetuses and neonates with DAA. Cardiac disproportion, abnormalities of the aortic arch or eccentric ductal jets should raise the possibility of a DAA and prompt further detailed imaging using the three-vessel view, which we have shown is particularly helpful in identifying DAA. The incidence of, and the relationships of DAA with blood group A, maternal diabetes, and possibly with SLE are still not clear. Given the ease with which the three-vessel view may be achieved, we suggest that a DAA represents another cardiac abnormality for which the three-vessel view is particularly helpful in the echocardiographic evaluation of the fetus. REFERENCES 1. Jan SL, Hwang B, Fu YC, Chai JW, Chi CS. Isolated neonatal ductus arteriosus aneurysm. Pediatr Cardiol 2002; 39: Lund JT, Hansen D, Brocks V, Jensen MB, Jacobsen JR. Aneurysm of the ductus arteriosus in the neonate: Three case reports with a review of the literature. Pediatr Cardiol 1992; 13: Hornberger LK. Editorial Comment: Congenital ductus arteriosus aneurysm. J Am Coll Cardiol 2002; 39: Better DJ, Timchak DM, Allan LD. Prenatal diagnosis of aneurysm of the arterial duct: Postnatal management and literature review. Cardiol Young 1997; 7: Puder KS, Sherer DM, Ross RD, Silva ML, King ME, Treadwell MC, Romero R. Prenatal ultrasonographic diagnosis of ductus arteriosus aneurysm with spontaneous neonatal closure. Ultrasound Obstet Gynecol 1995; 5: Mielke G, Peukert U, Krapp M, Schneider-Pungs J, Gembruch U. Fetal and transient neonatal right heart dilatation with severe tricuspid valve insufficiency in association with abnormally S-shaped kinking of the ductus arteriosus. 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6 62 Jackson et al. 7. Benson CB, Brown DL, Doubilet PM, DiSalvo DN, Laing FC, Frates MC. Increasing curvature of the normal fetal ductus arteriosus with advancing gestational age. Ultrasound Obstet Gynecol 1995; 5: Brezinka C. Fetal ductus arteriosus How far may it bend? Ultrasound Obstet Gynecol 1995; 6: Dyamenahalli U, Smallhorn JF, Geva T, Fouron J-C, Cairns P, Jutras L, Hughes V, Rabinovitch M, Mason CAE, Hornberger LK. Isolated ductus arteriosus aneurysm in the fetus and infant: A multi-institutional experience. J Am Coll Cardiol 2000; 36: Yoo SJ, Lee YH, Kim ES, Ryu HM, Kim MU, Choi HK, Cho KS, Kim A. Three-vessel view of the fetal upper mediastinum: An easy means of detecting abnormalities of the ventricular outflow tracts and great arteries during obstetric screening. Ultrasound Obstet Gynecol 1997; 9: Yagel S, Cohen SM, Achiron R. Examination of the fetal heart by five short-axis views: A proposed screening method for comprehensive cardiac evaluation. Ultrasound Obstet Gynecol 2001; 17: Yagel S, Arbel R, Anteby EY, Raveh D, Achiron R. The three vessels and trachea view (3VT) in fetal cardiac scanning. Ultrasound Obstet Gynecol 2002; 20: Vinals F, Heredia F, Guiliano A. The role of the three vessels and trachea view (3VT) in the diagnosis of congenital heart defects. Ultrasound Obstet Gynecol 2003; 22: Yoo SJ, Min J-Y, Lee YH, Roman K, Jaeggi E, Smallhorn J. Fetal sonographic diagnosis of aortic arch anomalies. Ultrasound Obstet Gynecol 2003; 22: Tan J, Silverman NH, Hoffman JIE, Villegas M, Schmidt KG. Cardiac dimensions determined by cross-sectional echocardiography in the normal human fetus from 18 weeks to term. Am J Cardiol 1992; 70: Lund JT, Jensen MB, Hjelms E. Aneurysm of the ductus arteriosus: A review of the literature and the surgical complications. Eur J Cardiothorac Surg 1991; 5: Acherman RJ, Siassi B, Wells W, Goodwin M, DeVore G, Sardesai S, Wong PC, Ebrahimi M, Pratti-Madrid G, Castillo W, Ramanathan R. Aneurysm of the ductus arteriosus: A congenital lesion. Am J Perinatol 1998; 15:
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