Development of the Ductus Arteriosusin Right Ventricular Outflow Tract ObstructionMARCO A. SANTOS, M.D., JORGE N. MOLL, M.D., CANTIDIO DRUMOND, M.D.,

WASHINGTON B. ARAUJO, M.D., NORIVAL ROMAO, M.D., AND NELSON B. REIS, M.D.

SUMMARY We studied the morphology of the ductus arteriosus in 14 infants, ages 2-90 days. Eight (group1) had pulmonary atresia (structural and functional) with an intact interventricular septum; six (group 2) hadpulmonary atresia with a ventricular septal defect. The inferior angle of the ductus arteriosus at the aorticjunction was measured in each patient. In group 1, this angle was obtuse in all but one patient. In group 2, theangle was acute in all. Further study of intracardiac anatomy suggested that in group 1, the obtuse inferiorangle of the ductus arteriosus was the result of a late and progressive obstructive phenomenon that allowed nor-mal right-to-left flow through the ductus arteriosus during much of fetal life. In group 2, the direction of ductusarteriosus flow (normally from the pulmonary trunk to the aorta) was reversed, and flowed from the aorta tothe pulmonary trunk. This reversal of flow was probably of early onset in the fetus, the aorta receiving the totalcombined ventricular output, and produced a small ductus arteriosus with an acute inferior angle. It is ex-tremely important not to rule out pulmonary atresia with an intact interventricular septum when aortographyin the newborn shows a normal-sized ductus arteriosus with an obtuse inferior angle. Despite existingpulmonary atresia, these patients have neither a hypoplastic right ventricle nor discontinuity of the right ventri-cle with the pulmonary artery.

THE IMPORTANCE of the development of the duc-tus arteriosus in congenital heart disease,'-3 par-ticularly in right ventricular outflow tract obstructionin which patency of the ductus is essential to life,4has recently been stressed. Although correct evalua-tion of the size of the ductus arteriosus in infants withpulmonary atresia is often difficult because constric-tion occurs shortly after birth, the ductus arteriosushas been described as a small structure that forms anacute inferior angle at its connection with the descend-ing aorta. However, these features differ from thosewe observed in a select group of patients who, despitehaving pulmonary atresia with an intact interven-tricular septum, on cineangiography had a normal-sized ductus arteriosus forming a normal obtuse in-ferior angle with the descending aorta. Theangiographic features and surgical prognosis of thesepatients must be differentiated from those of patientswith an underdeveloped ductus arteriosus, pulmonaryatresia and an intact interventricular septum.

In this report, we discuss the fetal development ofthe ductus arteriosus based on the time during fetallife at which the right ventricular outflow tractobstruction occurs, and on the consequent changesproduced in the fetal circulation. This knowledge isimportant in the correct management of this group ofhigh-risk patients.

Material and MethodsFourteen patients, 2-90 days of age, underwent

diagnostic hemodynamic and cineangiographic study(table 1). The interventricular septum was intact in

From the 6a. Enfermaria da Santa Casa da Misericordia, Rio deJaneiro, Brazil.

Address for correspondence: Marco A. Santos, M.D.; RuaHenrique Fleiuss, 262; Rio de Janeiro, 20.521, Brazil.

Received January 7, 1980; revision accepted March 31, 1980.Circulation 62, No. 4, 1980.

eight (group 1) and six had a ventricular septal defect(group 2). In group 1, the pulmonary valve was atreticin five (structural atresia) and three had evidence ofonly pinpoint patency of the pulmonary valve (func-tional atresia). There was right-to-left atrial shuntingin all. In group 2, all patients had pulmonary atresiaand a right-to-left shunt at the ventricular level. Thediagnosis was confirmed in all patients at necropsy orat surgery.We determined the inferior angle between the duc-

tus arteriosus and the descending aorta from theangiograms performed in the left anterior obliqueprojection, and compared these with angiograms ob-tained in full-term human newborn infants cathet-erized either to confirm the diagnosis of patent ductusarteriosus or to exclude congenital malformationssuspected clinically.

Results

Group 1

One patient (fig. 1) had a small, competent tricuspidvalve, a hypoplastic right ventricle and pulmonaryatresia. Myocardial sinusoids were well developed,and opacification of the aorta occurred through ananastomosis of the sinusoids with the right and leftcoronary arteries. The inferior angle of the ductusarteriosus was 30 (fig. 2). This patient had type Ipulmonary atresia by criteria of Davignon et al.6

In the other seven patients (fig. 2), the inferior angleof the ductus exceeded 90. In four (fig. 3) thepulmonary valve was atretic and in three (fig. 4) therewas evidence of pinpoint patency of the pulmonaryvalve with very faint opacification of the mainpulmonary artery. All had well-formed tricuspidvalves with mild-to-severe regurgitation. The rightventricular cavities were large, and myocardialsinusoids were absent. These patients had type IIpulmonary atresia by the criteria of Davignon et al.f

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DUCTUS DEVELOPMENT IN PULMONARY ATRESIA/Santos et al.

FIGLR[ 1. Patient I. (A) Right ventricularcineangiogram (anteroposterior pro]ection)showing a hypoplastic right ventricularcavity with myocardial sinusoids drainingvia the coronary arteries to the ascendingaorta (AAO0). (B) Left ventricular cine-angiograrn (left anterior oblique pro]ection).The diameters of the ascending aorta andthe aortic isthmus (IS) are larger than thedescending aorta (DA 0). The arrow in-

RVddicates the acute inferior angle between theLV ~~~~descending aorta and the narrow ductus

arteriosus (D). I infundibulum; LCAt coronar artery; LV left ventricle;RCA right coronary artery; RV rightventricle.

Group 2

In all six patients in group 2 (fig. 5), the right ven-tricular cavity was not hypoplastic. Only one patienthad tricuspid regurgitation. The inferior angle of theductus arteriosus was less than 500 in all.

D'iscussion R

A narrow, tortuous ductus arteriosus with an acuteinferior angle at the junction of the aorta and the duc-tus arteriosus and a wide aortic isthmus are commonfeatures in patients with pulmonary atresia or severepulmonary stenosis.' These features were observed inonly one of eight patients with pulmonary atresia andintact ventricular septum (group 1), and in all thosewith a ventricular septal defect (group 2). Wetherefore considered that variations in intracardiac D[2sl) * DAl

\ . R / . n~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.........~~~~~~~~~~~~30

o JFIGURE 3. Patient 5. (A) Right ventricular cineangiogram(anteroposterior projection) showing a normal-sized righ.ventricle (R V), moderate tricuspid regurgitation and nGnmocardial sinusoids. (B) Left ventricular cineangiogram

* INTACT VENTRCULAR SEPTUM (left anterior oblique projection) showing a ductus arteriosusO VENTRICULAR SEPTAL DEFECT (D) of normal size and configuration with an obtuse inferiorA PATENT DUCTUS ARTERIOSUS angle at the junction of the ductusarteriosus and the aorta

FIGURE 2. Measurements of the inferior angle of thejunc- (arrow). (C) Aortography after prostaglandin E, infusiontion of the ductus arteriosus and the aorta in patients with showing clearly the level of obstruction at the pulmonaryright ventricular outflow tract obstruction and in normal valve. AAO = ascending aorta; DAO = descending aorta,human newborns in whom the ductus arteriosus is still pa- I = infundibulum; IS = aortic isthmus; L V = left ventricle,tent. RA = right atrium.

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Voit 62, No 4, O(1013OB1 1980

TABLE 1. Heitodl!Ina?lic andl A nqiographih)Data

Age SAT (( ) r-essure (Torm Ilg) Tricuspid valvePt (days) SPex EA IA RA* LA8 1RVT IVt Size lRegullrgitat,iol

Group 11 2 M 71 72 7.5 7.5 98 60 Small Absent2 3 F 68 74 6.o 7.5 55 60 Large Severe3 30 AM 6 73 7.5 , 4.5 75) 45 Large Mild4 50 M 55:3 60 9g.5} 9.0 99 84 Large Mild5 1 M 51. 62 7.,5 6.0 70 r55 Large Mild6 3 F 64 72 7. r) 6.0 60 7r5 Large Severe7 30 F 71 80 7.,5 (.0 76 48 Large Severe8 30 F 64 69 7.0 6.5) 90 67 Large Mild

Group 29 30 1F 70 76 8.0 7.55)5 50 Large Mild

10 90 F 75 96 4.) 5.0 60 67 Large Absent11 2 Al .59 915 7.0o 6.5 4.5 48 Large Absent12 60 M 151 97 6.0 6.0 70 7r5) Large Absenit13 ,15 F 67 91 6.( 6.( 55 . Large Abseint,14 7 M 62 96 7.0 7.0 50 5( Large Absent*iMean pressure.tSystolic pressure.Abbreviations: A = aseendinig; I) = descendintig; I -isthlmuns;

HA -right atrium; BV =right ventricle SXT()SAtuatio0;Iiif infundibuluim;L; =+-= precent; absent.

left atrillul; Lv

anatomy could lead to major differences in the growthand development of the great arteries and ductusarteriosus in fetuses with pulmonary atresia.Group 1 included not only patients with structural

pulmonary atresia, but also those who showedevidence of pinpoint patency of the pulmonary valvewith only faint or no opacification of the pulmonaryartery. We classified these patients as having func-tional pulmonary atresia because all had essentially no

forward flow from the right ventricle and significantright-to-left shunting at the atrial level.

Although we did not classify the patients in thisgroup according to the size of the ventricular cavity,6only one of the eight patients had a hypoplastic rightventricle and a small tricuspid valve without evidenceof regurgitation. This, together with the developmentof large myocardial sinusoids, indicates the likelihoodthat blood did not pass freely from the right ventricleto the pulmonary artery during the greater part of thisinfant's fetal life.8 When obstruction to pulmonaryflow has been critical or complete from early in fetallife, the size and configuration of the ductus arteriosusshould reflect the small amount of aortic-to-pulmonary artery flow across the ductus arteriosus,and will differ from the normal ductus arteriosus,which acts as a continuous arch between the

FiGLwRI, 4. Patient 6. (A and B) Right ventricularcineangiograms (anteroposterior projection) showing theright ventricle (RV) in systole and diastole. The infun-dibulum (I) is markedly stenotic and there is severe tricuspidregurgitation. (C) Right ventricular cineangiogram (leftanterior oblique projection) showing faint early opacifica-tion of the pulmonary artery, indicating pinpoint patency ofthe pulmonary valve (arrow). (D) Left ventricularcineangiogram (left anterior oblique projection) showing aconstricted ductus arteriosus (D) with an obtuse inferiorangle (arrow). AA 0 -ascending aorta; DA 0 descend-ing aorta, IS aortic isthmus; LV = left ventricle; RAright atrium.

left venttricle;

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DUCTUS DEVELOPMENT IN PULMONARY ATRESIA/Santos et al.

TAnB3LE 1. (Continued(l)l{iglht velltricle Pulmnonary Aortic (liameter (min) Inferior angle

Cavity Inf Sinutlsoi(ds valve A 1 1) of ductus

Small Small + Atretic 2.5 1.7 1.0 300

Large Small - Atretic 2.2 1.7 1.4 1200

Large Small Atretie 1.8 1.2 0.8 1000Large Snall - Atretic 1.8 1.2 1.0 1100Large Small Atretic 2.0 1.5 1.0 1100Large Smnall P'inipoint 1.7 1.0 1.0 120`

Large Smrall Pinpoint, 1.4 1.1 0.9 1100Lairge Smnall Pinipoint 2.3) 1.6 1.4 1200

Jarge Srmall Atretic 10. 1.2 0.7 500Large Smalll Atretiei 2.5 1.3 1.1

VOL 62, No 4, OCTOBER 1980

had regurgitation. The aortic diameters had the sameproportions as in group 1, but the ductus arteriosuswas not normally developed, and the inferior anglewas acute in all patients.8 These features suggest thatthe right ventricular outflow tract obstruction oc-curred early in fetal life, but the ventricular septaldefect permitted the flow of blood from the right ven-tricle to the left ventricle and aorta, and therefore didnot significantly affect right ventricular development.The configuration of the ductus arteriosus indicatedflow from the aorta to the pulmonary trunk for a con-siderable portion of gestation.

These observations are important for correctdiagnosis and surgical management of these patientsand for understanding the developmental process.Although none of our patients underwent aor-tography, this approach is being used more and morefrequently in the diagnostic investigation of cyanoticnewborn infants.10 The angiographic features of anormal-sized ductus arteriosus with an obtuse inferiorangle do not exclude the possibility of pulmonaryatresia.The size of the right ventricular cavity and the level

of atresia, whether valvar or infundibular or both,may have important surgical and prognosticsignificance, although this is still a controversial sub-ject.8 11, 12 Freedom et al.'3 used a technique that per-mits simultaneous opacification of the right ventricleand the pulmonary artery, thereby obtaining betterdefinition of the level and site of the atretic segment.The patients who had a normally developed ductusarteriosus almost certainly maintained blood flowfrom the right ventricle to the pulmonary artery dur-ing a large part of fetal life. Consequently, they showneither a hypoplastic right ventricle nor discontinuitybetween this cavity and the pulmonary artery, becausethe atretic segment is localized at the valvar level.

In conclusion, patients with right ventricular out-flow tract obstruction do not always have an un-derdeveloped ductus arteriosus with an acute inferiorangle. We have described infants with pulmonaryatresia with intact interventricular septum and a nor-mally developed ductus arteriosus. In these infants,the obstructive phenomenon probably developed latein fetal life.

Acknowledgment

We are indebted to Dr. Elisabeth Gracie for her helpful review ofthe manuscript and to Wilcineia Nogueira for her secretarialassistance.

References1. Heymann MA, Rudolph AM: Effects of congenital heart dis-

ease on fetal and neonatal circulation. In Neonatal HeartDisease, edited by Friedman WF, Lesch M, Sonnenblick EH.New York, Grune & Stratton, 1972, p 70

2. Rudolph AM: Congenital Diseases of the Heart. Chicago, YearBook Medical Publishing Co, 1974, p 368

3. Rudolph AM, Heymann MA, Spitznas U: Hemodynamic con-siderations in the development of narrowing of the aorta. Am JCardiol 30: 514, 1972

4. Olley PM, Coceani F, Bodach E: E-type prostaglandins: a newemergency therapy for certain cyanotic congenital heartmalformations. Circulation 53: 728, 1976

5. Heymann MA, Rudolph AM: Ductus arteriosus dilatation byprostaglandin E1 in infants with pulmonary atresia. Pediatrics59: 325, 1977

6. Davignon AL, Greenwold WE, DuShane JW, Edwards JE:Congenital pulmonary atresia with intact ventricular septum.Clinicopathologic correlation of two anatomic types. Am HeartJ 62: 591, 1961

7. Jimenez MQ, Sarachaga IH, Granados FM, Martul EV, Van-jul IT, Dieguez CG, Diaz FA: Atresia pulmonar com tabiqueinterventricuar integro. Estudio de 28 casos. Arch InstCardiol Mex 46: 182, 1976

8. Miller GAH, Restifo M, Shinebourne EA, Paneth M, JosephMC, Lennox SC, Kerr IH: Pulmonary atresia with intact ven-tricular septum and critical pulmonary stenosis presenting infirst month of life. Investigation and surgical result. Br Heart J35: 9, 1973

9. Bharati S, McAllister AH, Chemmongkoltip P, Lev M:Congenital pulmonary atresia with tricuspid insufficiency:morphologic study. Am J Cardiol 40: 70, 1977

10. Sapin SO, Linde LM, Emmanouilides GC: Umbilical vesselangiocardiography in the newborn infant. Pediatrics 31: 946,1963

11. Dhanavaravibul S, Nora JJ, McNamara DG: Pulmonaryvalvular atresia with intact ventricular septum: problems indiagnosis and results of treatment. J Pediatrics 77: 1010, 1970

12. Bowman FO, Malm JR, Hayes CJ, Gersony WM, Ellis K:Pulmonary atresia with intact ventricular septum. J ThoracCardiovasc Surg 61: 85, 1971

13. Freedom MR, White RI Jr, Ho CS, Gingell RL, Hawker RE,Rowe RD: Evaluation of patients with pulmonary atresia andintact ventricular septum by double catheter technique. Am JCardiol 33: 892, 1974

CIRCULATION822

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M A Santos, J N Moll, C Drumond, W B Araujo, N Romao and N B ReisDevelopment of the ductus arteriosus in right ventricular outflow tract obstruction.

Print ISSN: 0009-7322. Online ISSN: 1524-4539 Copyright 1980 American Heart Association, Inc. All rights reserved.

is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231Circulation doi: 10.1161/01.CIR.62.4.818

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