Ultrasound Obstet. Gynecol. 5 (1995) 338-341 Fetal and transient neonatal right heart dilatation with severe tricuspid valve insufficiency in association with abnormally S-shaped kinking of the ductus arteriosus G. Mielke, J, Peukert*, M. Krapp', J. Schneider-Pungst and U. Gembruch* Departnent of Obstetries and Gynecology. University of Tabingen: *Department of Pediatrics, and ‘Division of Prenatal Medicine, Department of Obstetrics atid Gynecology, Medical University of Labeck: ‘Referring Obstetrician in private office, Flensburg, Germany Key words: Dorrer ECIOCARDIOGRAPHY, DUCTUS ARTERIOSUS, TRICUSPID VALVE INSUFFICIENCY, FETAL HEART, PRENATAL DiaGNosis| ABSTRACT Alterations of the ductus arteriosus, eg. ocelusion, come striction or aneurysm, can influence the fetal and neonatal circulation. A case of fetal right atrial and ventricular dilatation, severe tricuspid valve insufficiency and transient pulmonary valve regurgitation at 32 weeks of gestation is reported. Structural heart defects and extracardiac dis- cases (6. high output cardiac failure in arteriovenous shunts and anemia) were excluded by Doppler echocardi- ography and fetal blood sampling. An abnormally S-shaped inking of the ductus arteriosus with increased systolic and diastolic flow velocities inthe distal part was demonstrated. At 45 weeks’ gestation, Cesarean section was performed, hecause of increased tricuspid valve insufficiency, and a healthy boy was born. After barth, right heart dilatation ‘and tricuspid valve insufficiency decreased. The cardiac changes in relation 10 the anatomical abnormality of the ductus arteriosus are discussed. INTRODUCTION In addition to structural heart diseases, abnormalities of the fetal ductus arteriosus, such as occlusion demon- strated experimentally in lambs‘ or constriction during indomethacin therapy?, can cause right ventricular dilata- tion and tricuspid regurgitation. We present a case of fetal and transient neonatal right atrial and ventricular ilatation with severe holosystolic tricuspid valve insufi- ciency ir association with an abnormally S-shaped kink- ing of the ductus arteriosus and increased peak systolic and diastolic flow velocities in the fetal ductus arteriosus. METHODS Sonographic examinations were performed with a 3.5- MHz phased-array sector seanner (Acuson 128 XP-10 ‘Acuson Inc., Mountain View, California). Two-dimen- sional echocardiography was followed by color Doppler ow imaging, and spectral pulsed wave and continuous wave Doppler echocardiography. Atrial and ventricular dimensions were measured fiom the four-chamber view? To maintain the greatest reproducibility of the color Doppler display of regurgitant jet phenomena, the con- ditions of the examination were kept as constant as possible. We used the same 3.5-MHz transducer and a constant adjustment of the instrument settings with regard to the color Doppler transmitting power for fetal scanning, the pre-processing program, the small color Doppler gate setting tor optimizing hoth temporal (high frame rate) and spatial (axial and lateral) resolution, the color filter setting with a high degree of motion diserimi- nation and the selectable velocity-variance color map. The transinitting focal point was set as close as possible to the regurgitant jet. Two-dimensiowal imaging and Doppler recording of the ductus arteriosus were pet~ formed in a sagittal planc of the fetus (short axis of the fetal heart), showing the main pulmonary artery, bifur- cation, ductus arteriosus and descending aorta. Ductal waveforms were obtained at an angle of < 20° to flow and analyzed for peak systolic, diastolic and mean flow velocity. The pulkatihty index (PI) was calculated as (systolic velocity — diastolic velocity)’mean maximum velocity. Semi-quantification of tricuspid valve insuffi- ciency was performed by relating the temporal duration of the regurgitant jet to the entire systolic. period, measured by M-Q mode imaging (color Doppler Correspondence: Dr G. Mielke, Department of Obstetrics and Gynesology, University of Tubingen, Schecheatl 4, 7076 Tabingen, Germany 338 Received 25, Revie Accepted 27 194 2.95 295Abnormal ductus arteriosus M-mode echocardiography). The maximal spatial expan sion of the regurgitant jet was judged by measuring its length in color Doppler flow imaging in relation to the distance from the atrioventricular valve to the opposite atrial wall within the four-chamber view. Furthermore, again based on the four-chamber view. the maximal area of regurgitant jet in color Doppler flow imaging was related to the cross-sectional atrial area, both determined planimerrically’. The pressure gradient (mmHg) across the tricuspid valve was estimated by application’ of the modified Bernoulli equation AP = 4x V°, where V (iis) represents the peak velocity of the regurgitant jet CASE REPORT A.28-year-old woman (gravida 3, para 0), gestational age 32 weeks, with no history of medication during preg- nancy, particularly no [sympathomimetic agent and no indomethacin, was referred hecause of right atrial and ventricular dilatation and tricuspid regurgitation. A non- stress test was negative. Ultrasound examination demon- strated a fetus appropriate in size for westational age with normal movements and no evidence of hydrops. Doppler flow velocity waveform indices of the uterine arteries (PI 0.93 and 0.77, respectively, no notching), umbilical artery (PI 0.66) and middle cerebral artery (PI 1,60) were normal. The pre-load index, derived from inferior vena cava flow velocity waveforms, was in the upper normal range (0.30). Fetal echocardiography excluded a struc- tural heart defect. A marked dilatation of the right atrium (width 24mm, length 18mm) and ventricle (diastolic width Imm) (Figure 1), severe holosystolic tricuspid valve insufficieney (Figures 2 and 3) and transient pul- monary valve regurgitation (Figure 4) were observed. Left heart dimensions (atrial width 14 mm, atrial lergth 13 mm, diastolic ventricular width 12.mm) were in the normal range’. At the first examination, the tricuspid regurgitant jet had a peak flow velocity of 3.2 m/s, corresponding to a maximal pressure gradient of 41 mmHg, a jet length of 10 mm (right atrium 18 mm, ratio 0.6) and an area of 37 mm? (right atrium 320 mm, ratio 0.1). Pulmonary stenosis could be excluded by demonstrating normal blood flow velocities (0.82 m/s) and absence of a spectral broadening (‘disturbed” tlow) in the blood flow of the pulmonary trunk. An abnormally S-shaped kinking of the ductus arteriosus (Figure 5) was detected, Acceleration of peak systolic flow velocity in the distal ductal part up to 1.49 mis and peak diastolic velocity up to 0.26 mis (PI 2.62) was recorded (Figure 6) These are borderline elevated velocities related to ges- tational age"*. The peak systolic flow velocity in the ascending aorta was 1.22 m/s. Fetal blood sampling yielded normal findings (kary type 46.XY; hemoglobin 13.1 g/l; reticulocyte count, liver enzymes and albumin concentrations within the normal range; anticparvovirus, anti-B-19coxsackie- echovirus and anti-cytomegalovirus antibodies negative) At 35 weeks’ gestation, the color Doppler-derived spatial jet parameters of the holosystolic tricuspid regurgitation Mielke et al. increased (jet length 22 mm, right atrium 22 mm (ratio 1); area 80 mm’, right atrium 421 mm: (ratio 0.2)). Peak flow velocity in the regurgitant jet rose to 4.65 mis, corresponding to the maximal pressure gradient of 53 mmHg. The acceleration of systolic and diastolic peak flow velocities in the distal part of the S-shaped ductus arteriosus continued (systolic 1.55 m/s diastolic 0.24 mis, PI 2.46), At 35 weeks +6 days, Cesurean section was performed afier assessment of fetal pulmonary matura- tion by amniocentesis, because of progressively severe holosystolic tricuspid valve insufficiency. A healthy boy with a weight of 2530 g was born. Laboratory findings ‘were normal, Chest X ray examination revealed a dilated heart. Right heart dilatation and holosystolie tricuspid valve insufficiency with a maximal pressure gradient of 41 mmHg persisted temporarily, as demonstrated by echocardiography 7 h after birth. At this time, the ductus arteriosus was already closed and there was no inter atrial blood shunting. During the next few days. right heart dilatation and tricuspid regurgitation decreased. Thickening of the right ventricular papillary muscles was diagnosed. Right ventuicular dilatation had resolved by the 3rd day postpartum, Mild tricuspid valve regurgita- tion was present at this time. There was no clinical or cchocardiographie evidence of persistent pulmonary hypertension or persistent fetal circulation, DISCUSSION Right ventricular dilatation and tricuspid valve insuffi ciency in addition to structural heart diseases can be caused by alterations in the ductus arteriosus, Acute fetal ductal occlusion in lambs results in a rise in pulmonary arterial pressure, right ventricular dilatation, reversible tricuspid regurgitation, decreased right ventricular out- put, increased left ventricular output and a fall in combined cardiac output'. Indomethacin given to the pregnant ewe causes constriction of the ductus arteriosus, fetal pulmonary arterial hypertension, pulmonary arteri- olar changes and right ventricular damage, with degenerative myocardial changes in the tricuspid valve papillary muscles, the right ventricular free wall and the interventricular septum’. Considering these findings, in- trauterine constriction of the ductus arteriosus may be ‘one cause of persistent pulmonary hypertension or per- sistent fetal circulation of the newborn infant. permanent fr transient tricuspid insufficiency and neonatal myo- cardial ischemia? Doppler ultrasound provides flow velocity data from the fetal ductus arteriosus as carly as II weeks of gestation!” Recent studies have established the dis tribution of ductal flow parameters from I1 weeks of gestation to term’, An increase of ductal peak systolic and diastolic flow velocity with advancing gestational age was found. There was no correlation with fetal heart rate’. Ductal flow parameters are modhlated by fetal behavioral states" and fetal breathing movements" Doppler echocardiography is a sensitive tool for the detection of fetal ductal constriction, characterized by an Ultrasound in Obstetrics and Gynecology 339Abnormal ductus arteriosus Figure 1 Fetal dilatation of the right atrium (RA) and right ventricle (RV) with severe tricuspid valve insufficiency Figure 2 Color Doppler M-mode: holosystolic tricuspid valve insufficieney (blue with aliasing) and right ventricular inflow (red) Figure 3. Holosystolic tricuspid valve insufficiency (continu bus wave Doppler) with peak flow velocity of 3.65 mis increase in peak systolic and diastolic low velocities of more than 1-4 m/s and 0.3 mvs, respectively in the ductus arteriosus”, and low pulsatility index’. The low pulsatil- ity index (1.25 + 0.16) is able to distinguish ductal con- on from increased right ventricular output (PL 3.11 40.46) in eases of increased ductal flow velocities In the human fetus, transient ductal constriction with and without tricuspid regurgitation caused by indo- tethacin therapy in the mother has been demonstrated 340 Ultrasound in Obstetnes and Gynecology Mielke et al. Figure 4 Pulmonary valve regurgitation (red). RV. right ven- tricle; PA, pulmonary artery Figure $_ Pulmonary artery (|) bifurcation and S-shaped kink- ing (arrow) of the ductus artoriosus 2) Figure 6 Ductal velocity waveforms (pulsed wave Doppler) Acceleration of peak systolic flow velocity in the distal part up {0 1.55 misand peak diastolic velocity up (00.24 mis{pulsatility index 2.46) by Doppler cchocardiography*!* ". Constrictive effects of glucocorticoids on the human fetal ductus arteriosus seem to be a possibility, but this is controversial’®" In the reported case, the fetus showed right atrial and ventricular dilatation, severe holosystolie tricuspid insufTiciency and transient pulmonary valve regurgita tion. There was no evidence of structural heart detect left or right ventricular outflow obstruction, medication- induced ductal constriction. or increased right ventricularAbnormal ductus arteriosus output, Extracardiae diseases could be excluded (e.g. high cardiac output failure in arteriovenous shunts and anemia). An abnormally S-shaped kinking of the ductus arteriosus with borderline increased peak systolic and diastolic flow velocities in the distal kinked part could bbe demonstrated. The pulsatility index was in the normal range’, In all probability, the anatomical abnormality of the ductus arteriosus caused pulmouary regurgitation, fetal and transient neonatal right ventricular dilatation and functional holosystolic tricuspid valve insufficiency, similar to the cardiac changes demonstrated in ductal constriction. The elevated peak systolic flow velocity in the ascending aorta (1.22 mvs) may have been caused by increased left ventricular output due to right-to-left shunting across the foramen ovale and increased pulmo- nary arteriolar flow! Structural abnormalities of the ductus arteriosus seem to be rare®. Congenital aneurysms have been demon- strated in the fetus and infant’, Agenesis of the ductus arteriosus is usually associated with absent pulmonary valve syndrome, To our knowledge, the abnormality of the ductus arteriosus described here has not previously been published elsewhere, On the basis of present evidence, we recommend careful evaluation of the ductal anatomy and of ductal hemodynamies in cases of fetal and neonatal right ventricular dilatation and tricuspid or pulmonary valve insufficiency. If these findings are associated with an abnormal S-shaped kinking of the ductus, prompt delivery may result in spontaneous resolution of the condition ACKNOWLEDGEMENT The authors would like to thank Mrs Regina Pompe for secretarial assistance in preparation of the manuscript. REFERENCES, |. Tulzer, G., Gudmundssan, $., Ratondo, KM, Wood. D.C, Yoon, G. ¥. and Huhta, J.C, (1991). Acute fecal ductal occlusion in lambs. Am, J. Obstet. Gynecol., 168, 115-8 Eronen, M., Pesonen, E., Kurki, T., Ylikorkala, O, and Hallman, M. (1991) ‘The effects of indomethacin and a B-sympathomimetic agent om the fetal ductus arteriosus during treatment of premature labor: A randomized double blind study. Am. J. Obstet. Gynecol. 164, 141-6 3. Tan, J, Silverman, N.HL, Hoffmann, J. 1. E, Villegas, M. and Selmidt, K. G (1992), Cardiac dimensions determined by cross-sectional echocardiography in the normal huaan fetus from 18 weeks to term. Amt. J. Cardiol, 70, 1459-67 4, Gembruch, U., Redel, D. A., Bald, R. and Hansmann, M. (1993). Longitudinal study in 18 cases of fetal supraventric« tlar tachycardia. Doppler echocardiographic findings and pathophysiologic implications. Am. Heart J., 25, 1290-301 5. Malle, L., Brubakk, A., Tromsdal, A. and Angelsen, B. (1978). Noninvasive assessment of pressure drop in mitral stenosis by Doppler ultrasound. Br. Heart J., 40, 131-40 6. Kanzaki, T-and Chiba, Y. (1990) Evaluation of the preload condition of the fetus by inferior vena caval blood flow patter. Feral Diagn. Ther. §, 168-74 1 10. Mielke et al vd Mooren, K., Barendregt, L. G_and Wladimiroff, J. W. (1991). Flow velocity waveforms in the human fetal ductus arteriosus during the second half of pregnancy. Pediatr Res.. 30, 487-90 Tulzce, G., Gudmundsson, S., Sharkey, A.M., Wood, D.C, Cohen, AW. and Huhta, J.C. (1901). Doppler echocardiography of fetal ductus ateriosus constriction versus increased right ventricular output. J. dm. Coll Cardiol. 18, 532-6 Levin, DL, Mills, L.J. and Weinberg, A.G. (1979). Hemodynamic, pulmonary vascular, and myocardial ab- normalities secondary to pharmacologic constriction of the fetal ductus arteriosus, Circulation, 60, 360-4 Brezinka, C.. Huisman, T. W. H.. Sujnen, T. and Wladi- smiroff, J. W, (1992), Normal flow velocity waveforms in the fetal ductus arteriosus inthe first half of pregnancy. Ultra. sound Obstet. Gynecol, 2, 397-401 Brezinka, C., Gittenberger-de Groot, A. C. and Wladimi off, J.W. (1993). The fetal ductus arteriosus, a review. Zentralbl. Gynakol, 115, 423-32 Brezinka, C., Stjjnen, T. and Wiadimiroff, 1 W, (1994) Doppler flow velocity waveforms in the fetal ductus areri- ‘sus during the first half of pregnancy: a reproducibility study. Ultrasound Obstet. Gynecol., 4, 121-3 vd Mooren, K., v Eyck, J. and Wiadimiroff, J. W. (1989). Human fetal ductal flow velocity waveforms relative to behavioral states in normal term pregnancy. Am. J. Obstet Gynecol, 160, 3714 v Eyck, J., vd Mooren, K. and Wladimiroff, J. W. (1990). Ductus arteriosus flow velocity modulation by fetal breath= ‘ng movements as a measure of fetal lung development. Am J. Obstet. Gynecol, 163, 558-66 Huhta, J.C, Moise, K.J., Fisher, D.J., Sharif, D.S., Wasserstrum, N_ and Marin, C. (1987). Detection and {quantitation of constiction ofthe fetal ductus arteriosus by Doppler echocardiography. Circulation, 75, 406-12 Moise, K. J., Hubta, J.C. Sharif, D. ., Ou, C.N., Kir- shon, B., Wasserstrum, N. and Cano, L. (1988). In domethacin in the treatment of premature labour ~effects| com the fetal ductus arteriosus. N. Engl J. Med.,319, 327-31 Mari, G., Moise, K. J., Deter, R.L., Kirshon, B., Huhta, J.C. Carpenter, R, J. and Cotton, D. B. (1989). Doppler assessment of the pulsatility index of the middle cerebral artery during constriction of the fetal ductus arteriosus after indomethacin therapy. mm. J. Obstet. Gynecol, 161, 1528-31 Wasserstrum, N., Hubta, J.C.. Mari, G., Sharif, D. S., Willis, R. and Neal, N. K. (1989), Betamethasone and the human fetal ductusarterioaus. Obster Gynecol. 72, 897-9) Eroneu, M., Kati, A., Pesone, E. aud Hallinan, M, (1993), The effects of antenatal dexamethasone administration on the fetal and neonatal ductus arteriosus. Am. J. Dis, Child, 147, 187-92, Recker, AF. and Anderson, RH. (1986). Pathology of Congenital Heart Disease, pp. 349-56. (London: Butter- worths) Lund, J.T. Hansen, D., Brocks, V.. Jensen, M. B. and Jacobsen, JR. (1992). Aneurysm of the ductus arteriosus jn the neonate: three case reports with a review of the literature, Pedr. Curdiol, 13, 222-6 2. Jesseph, J. M., Mahony, L., Girod, D. A. and Brown, J. W. (985). Ductus arteriosus aneurysm in infancy. Ann. Thorac. ‘Surg, 40, 620-2 Emmanquilides, GC, Thanopoulos, B., Siassi, B. and Fishbein, M. (1976). ‘Agenesis’ of ductus arteriosus ase sociated with the syndrome of tetralogy of Fallot and absent pulmonary valve. Am, J. Cardiol. 37, 403-9 Entedgui, J. A., Sharland, G. K., Chita, S.K., Cook, A., Fagg, Nand Allan, I.. (1990). Absent pulmonary valve syndrome with venticular septal defect. Role of the arterial duct. dm. J. Cardiol, 66, 233-4 Ultrasound in Obstetrics and Gynecology 341