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Origin of the right pulmonary artery from the aorta
Origin
of the Right
Pulmonary
/
Artery
from the Aorta A Clinical-Pathologic
Study of Two Types Based on
Caliber of the Pulmonarv
J
Arterv* J
SHIRLEY L. KAUFF~IAN, M.D., ALICE C YAO, M.D., CAROLYN B. WEBBER, M.D. and JOSHUA LYNF~ELD, M.D., I;.A.c.c. Brooklb-n,
0
RIGIN of the right pulmonary artery from the aorta is a rare malformation of the arch system’ in which the right lung is perfused by the systemic and the left lung by the pulmonic circulation.2-4 Pulmonary hypertension may occurI,* and seems to be an important complication in those infants who die in the first year of life. The main anatomic types of isolated origin of the right pulmonary artery from the aorta seen in this group of infants are those in which the artery arises from the ascending aorta and those in which a brachiocephalic vessel supplies the right lung (Groups 7 and 9 of the classification of Pool et al.‘). The differences between these anatomic types are also reflected in the development of the pulmonary vasculature of the two lungs. In the case described by Anderson and colleagues,2 which they considered as proximal interruption of the pulmonary arch, the right pulmonary artery arose from the innominate and became obliterated, and the arteries in the right lung were thin-walled compared with the left lung. Rubin and Strauss3 and Wagenvoort and co-workersblater described somewhat similar cases in which the right pulmonary artery was narrowed or obliterated after its origin near the innominate ; here, was relative too, there atrophy of pulmonary arteries in the right lung and medial hypertrophy of arteries in the left lung. When the right pulmonary artery arose directly from the ascending aorta, without a
iVew York
narrowed -,egment, as in cases described by Griffiths et a1.,4 both lungs received excessive blood flow, and there was pathologic evidence of bilateral pulmonary hypertension. The explanation for the differences between these two forms of origin of the right pulmonary artery from the aorta is seen in the different embryologic origin of the two types.lb2 In tr-le absence of the right pulmonary artery, in which the right lung is supplied by a brachiocephalic vessel, Pool et al.’ considered that the vessel represents persistence of the ductal portion of the pulmonary arch. Wagenvoort and co-workers5 shared this interpretation and believed that the stenosis or atresia of the “right pulmonary artery” when it arises from a brachiocephalic vessel is due to the inherent tendency of ductal tissue to close. When the right pulmonary artery arises directly from the ascending aorta, it is considered a normal but displaced artery’ and as such would have no tendency to close. All of these studies suggest that it is largely the tendency of the artery to close that determines the size of the aortic-pulmonic connection, which, in turn, accounts for alterations in blood ~Iow’~~~~~~ and in the newborn, alterations in pulmonary vasculature. We present a case report of isolated origin of the right pulmonary artery from the aorta and a review of autopsy cases in infants which emphasizes the relationships of location of the right pulmonary artery, size of aortic-pulmonic communication and development of pulmonary
* From the Departments of Pathology and Pediatrics, State University of New York Downstate Medical Center, and Kings County Hospital, Brooklyn, N. Y. VOLUME
19,
MAY
1967
741
Kauffman, vasculature. may
Certain
help
to
clinical
differentiate
Yao,
featrrres*~” the
two
Webber
and
Lynfield
which
groups
are
also included. C.4s~
KEPORT
A 2 month old Negro female infant was admitted to Kings County Hospital on Sept. 20. 1964, because of difficulty in breathing. She was the product of a full term uncomplicated pregnancy, the first of an 18 year old mother. Birth weight was 5 lbs., 7 oz. No abnormalities were noted until four days prior to admission, when a cough and then respiratory distress developed. Physical Examination: The infant was well develWeight was oped and had mild, diffuse cyanosis. 8 Ibs., height 47 cm., pulse rate 152/min. and respiratory rate lOO/min. Blood pressure was 70/40 mm. Hg in the right arm and 80/50 in the right leg. Radial and femoral pulses were normal. The left precordium was prominent with a visible impulse, and the maximal palpable impulse was at the fourth intercostal space, 2 cm. beyond the left mid-clavicular line. The first heart sound was normal, and the second, single, and accentuated at the upper left sternal border. A grade 3-4/6 crescendo, almost pansystolic murmur was heard best along the lower left sternal border. Fine crepitant rales were heard at the left lung field posteriorly. The liver edge was palpable 4.5 cm. below the right costal margin. The nail beds were slightly cyanotic. Laboratory Data: Hemoglobin was 15 gm./lOO ml., white blood count 17,100 with 62yc neutrophils, 220/, lymphocytes, 14% monocytes and 2 eosiniphils. Roentgenograms of the chest (Fig. 1) showed moderate cardiomegaly, decreased vascular markings over the right lung field and increased markings over the left lung. The interspaces on the right were slightly narrower than on the left, and the right hemithorax
“I FIG. 2. atria1
Electrocardiogram and right ventricular
are
1.
Chest
narrowing
roentgenogram.
compared of the interspaces
hyperlucent
Lung
fields
with the left, on the right.
on
and
the
right
there
is
“5
“6
compatible with severe hypertrophy.
right
appeared smaller than the left. l‘he electrocardiogram (Fig. 2) showed a regular sinus rhythm with a rate of lbO/min., axis +150”, tall peaked P waves in lead II, S-T elevation in precordial leads and diphasic The electrocardiogram was interpreted as T in VI. indicating right axis deviation and severe right atria1 and ventricular hypertrophy. Hospital Course: The infant was placed in an oxygen croupette with mist and received digoxin and Mercuhydrin@ for heart failure and penicillin and Kantrex@ for possible pneumonia. She continued to have dyspnea and cyanosis, but from the fourth hospital day on showed slight but definite improvement. However, before any further diagnostic studies could be done, hematemesis with signs of intestinal obstruction developed, and the infant died. The diagnosis of absent right pulmonary artery with pcor collateral circulation was considered on the basis of chest roentgenogram. SUMMARY
FIG.
“2
OF
SIGNIFICANT
POSTMORTEM
FINDINGS
The heart (Fig. 3) lay in an oblique position with the right ventricle comprising the apex. The right atrium was extremely dilated and hypertrophied. It received a large superior vena cava, dilated coronary sinus and inferior vena cava. The foramen ovale was adequately covered by the septum primum but could be probed to a maximal diameter of 1.0 cm. The right ventricular cavity was dilated, and both the trabecular and compact myocardium were hypertrophied. A dilated pulmonary valve contained three normal cusps. The large main pulmonary artery, which was dilated above the valve, narrowed somewhat at the origin of a large, thickwalled ligamentum arteriosum and continued as the left pulmonary artery. The right pulmonary artery was absent. Four pulmonary veins entered a small left atrium. No abnormalities of the tricuspid, mitral, pulmonic: or aortic valve were present. The ventricular septum was intact. The valve and heart THE
AMERICANJOURNALOF
CARDIOLOGY
Origin
of Right
Pulmonary
Artery from Aorta
743
changed to a thin-walled vessel bvhirh graduall! dilated to a maximal circumference of 7 mm. at the hilum of the right lung where it gave off branches to three lobes. The remaining branches of the aorta were normal. ‘l-he right lung was also supplied by one large bronchial artery and intercostal arteries. The left lun,g was larger than the right and was dark red and firm. Prominent pleural vessels were seen over the right lung. A superficial gastric erosion was found on the lesser curvature of the stomach, and the upper 70 cm. of the jejunum was distended, purple and contained dark bloody fluid. MICROSCOPIC
EXAMINATION
Sections from all lobes of both lungs were examined. There was a striking difference between the two sides. Elastic and muscular pulmonary arteries of the left lung showed severe medial hypertrophy and elastosis (Fig. 4A), while those of the right lung were extremely thin walled (Fig. 4B). Many arteries of the right lung had only a thin rim of muscularis between the internal and external limiting membranes, and in others no muscularis was identified. The mean ratio of media to total diameter of arteries less than 100 p was 15.7 per cent in the left lung and 4.1 in the right lung. The mean ratio of arteries of 8 matched control infants without heart or lung disease was 4.6yo f 1.6. Sections of the main pulmonary artery showed the expected fetal elastica pattern and moderate intimal thickening. Sections taken at the origin of the anomalous right pulmonary artery showed parallel bands of elastic tissue continuous from the aorta into this At the narrow mid-portion of the artery (Fig. vessel. 5A), the elastica was fragmented, and the arrangement of bundles of smooth muscle was similar to that found in the left ligamentum arteriosum. There was no intimal thickening. Distally, the vessel resembled the intramural pulmonary artery (Fig. 5B). The left Lungs:
Fro. i.
I)r.Iwina or hrart. lungs and great vessels shows the anomalcrus right pulmonary artery arising just proximal to the innominate artery. It enters the hilum at the arrow. The right pulmonary artery narrows to 3 mm. in circumference at the point whve it is crossed by a prominent azygos vein. The right lung is smaller than the left. The right atrium and right ventricle are dilated and hypertrophied. The ductus arteriosus, which appears large externally, is closed.
measurements were as follows: tricuspid 6.0 cm., pulmonary 2.5 cm., mitral 3.0 cm. and aortic 2.0 cm. in circumference; the right ventricle and left ventricle each measured 5 mm. in thickness. The jirst aortic branch was an artq to the right lung which arose 2.5 cm. distal to the aortic valve immediately inferior to the innominate artery (Fig. 3). At its origin the right pulmonary artery measured 6 mm. in circumference and was thick-walled. It narrowed abruptly to 3 mm. in circumference where it was crossed by the azygos vein. Past the point of crossing, the right anomalous pulmonary artery abruptly
A
B
FIG. 4. A, a thick-walled pulmonary artery representative of those in the left lung shows medial hypertrophy and elastosis. (Verhoeff-Van Gieson X 250.) B, typical thin-walled intrapulmonary artery in the right lung; many other small arteries contained no recognizable media. (Verhoeff-Van Gieson X 250.) VOLUME
19.
MAY
1967
744
Kauffman,
Yao, Webber
and Lynfield
n
A
FIG. 5. A, longitudinal section of the right pulmonary artery along the region of narrowing. The lumen of the artery is to the right. Note thick, fragmented elastica and arrangement of muscular-is resembling ductus arteriosus. (Verhoeff-Van Gieson X 70.) B, right pulmonary artery distal to narrowed segment shows a normal configuration of elastica for this age. (Verhoeff-Van Gieson X 70.)
ductus arteriosus was closed and showed intimal liferation and zones of calcification (Fig. 6).
REVIEW
FIG. 6. Cross section of (Verhoeff-Van artel riosum.
normal Gieson
X
left ligamentur n 15.)
OF
pro-
THE LITERATURE AND DISCUSSION
Tables I and II summarize 16 autopsy cases of isolated origin of the right pulmonary artery from the aorta in children. References to many interesting cases in earlier literature which involve both adults and children in whom a diagnosis was made clinically can be found elsewhere.6~s~10-13 We excluded these cases because they contained too few details for analysis. Table I summarizes the major findings in patients whose right pulmonary artery arose in the vicinity of the innominate artery (Group l), and Table II summarizes the cases of those patients whose right pulmonary artery arose from the ascending aorta (Group 2). There were 8 patients in each group, and 6 in each group died before the age of 5 months. THE
AMERICAN
JOURNAL
OF CARDIOLOGY
Origin
of Right
Pulmonary
Artery
TABLE
Origin of the Right
Age at Death
C:ase No. Reference 1ip
SeX
6 days
22
Pulmonary
I
Artery from the Aorta (Vicinity Vascular Markings Roentgenogram
ECG
F
.
14 mo.
M
RAD RAE RVH
L. > R.
745
from Aorta
of the Innominate
---------Autopsy Small Pulmonary :\rteries I,. R.
-----
Heart LVH RVH
”
‘.
RVH
H
D
.Irtery)
(Group
1)
Findings-----------~ Right Pulmonary Artery Origin Circ.* Innom.
0 ‘)5 cm.
Innom.
Oblit.
312
6 wk.
M
RVH
L. > R.
RVH
Prox. to innom.
0.2 cm.
43
4 mo.
M
RAD RVH
N
RVH
H
D
Prox. to innom.
Oblit.
56
3 wk.
F
RVH LVH
H
D
Base of innom.
“Narrow”
66
14 mo.
M
.. .
RAH RVH
;,
?
Innom.
“Pin-point”
7”
2 mo.
M
RAH RVH
L. > R.
RAH RVH
H
N
Base of innom.
“Quite small”
8
2 mo.
F
RAE RVH
L. > R.
RAH RVH
H
D
Base of innom.
0.3 cm.
(present case)
N
_.
_,
* Circumference of narrowest portion. LVH = left ventricular hypertrophy; L. = left; R. = right; RVH = right ventricular hypertrophy; Innom. = H = hypertrophied; D = dilated; innominate artery; RAD = right axis deviation; RAE = right axis elevation; Oblit. = obliterated; Prox. = proximal; RAH = right atria1 hypertrophy; N = normal. TABLE
Origin of the Right
Pulmonary
Vascular Markings Roentgenogram
II
Artery from the Ascending Y-Autopsy
Sex
913*
4 mo.
F
NAD
Increased
RVH LVH
10’7
2 mo.
F
RAE RVH LVH
Increased
LVH LAD LVD
114
6’/2 mo.
F
NAD LVH RVH Tall P
Prominent
RVH LVH
H
EGG
Heart
2)
Findings------~ Small Pulmonary Right Pulmonary Arteries Artery L. Origin Circ. R.
Age at Death
Case No.
Aorta (Group
“No difference”
H
Ductus
Aorta (L.) Aorta (R.)
2.7 cm.
Cl
l.Ocm.
0
Aorta
3.7 cm.
Cl
(post.)
124
33 mo.
M
RAD RVH Tall P
Prominent
RVH LVH
H
H
Aorta (R.)
3.5 cm.
Cl
13i8
25 days
M
RVH
Prominent R. > L.
RVH
“N”
“N”
1.3cm.
0
146
2 mo.
M
RAH RVH
Increased R. > L.
RVH RAH
“N”
“N”
Aorta (R.) Aorta
0.7 cm.
Cl
156
2 mo.
F
LVH
Increased R. > L.
LVH
“Large”
0
16’9
14 wk.
M
RVH
Increased
“Large”
0
.
“N”
H(F)
“Similar”
Aorta (R.) Aorta (post.)
* Also reported as Maier case 310 and Griffiths case 1.4 Abbreviations same as Group 1; in addition: 0 = open; posterior. VOI LIME
19:
MAY
1967
Cl = closed (anatomically
or physiologically)
; post. =
Kauffman, CLINICAL
Yao,
Webber
FEATURES
In both groups, respiratory distress, cyanosis, pulmonary hypertension and intractable congestive heart failure developed in the infants in the first weeks or months of life. Chest roentgenograms showed cardiomegaly in patients of both groups, but often differences were noted in pulmonary vascular markings.8-11 In Group 1 the vasculature of the right lung was diminished, while that of the left was normal or increased (Cases 2, 3, 7 and 8). Since the blood flow to the right lung is decreased in cases of stenosis or atresia of the right pulmonary artery, the right hemithorax, as well as the right lung, may be smaller than the left (Cases 2, 4 and 8). In Group 2 cases, by contrast, the pulmonary vasculature was often increased or prominent on both sides, or the right lung had increased vascular markings. The right and left lungs in Group 2 cases were the same size. Review of available electrocardiograms showed a constancy of signs of right atria1 and right ventricular hypertrophy in Group 1 cases. In patients whose pulmonary artery arose from the ascending aorta (Group 2), there were variable patterns from pure right to left ventricular or biventricular hypertrophy. These differences reflect the different hemodynamics in the two groups. In patients of both groups the left lung received the total output of the right ventricle under systemic pressure. This increased flow and pressure, probably accompanied by vasoconstriction,3 may be important in delaying the normal regression of the fetal pattern of the muscular arteries in these small infants. In Group 2, where a wide communication between the aorta and right pulmonary artery was maintained, the right lung also received blood under systemic pressure, and left ventricular hypertrophy eventually ensued. In addition, in some of these patients the ductus arteriosus was patent. PATHOLOGIC
FEATURES
Group 9: In the 8 patients whose right pulmonary artery arose from or adjacent to the innominate artery (Table I), 7 showed a stenotic or atretic segment in the pulmonary artery. Often the artery was funnel-shaped, with the maximal narrowing in the center and flaring on either side. The exact caliber of the stenotic artery was not given in most cases, but the vessel was extremely narrow and in 2 instances was atretic. It is interesting that the youngest
and
Lynfield
infants had patent vessels, while the oldest had vessels with pinpoint (Case 6) or atretic lumens (Cases 2 and 4). Though the small pulmonary arteries were not always completely described, it was possible in many cases to recognize the differences in media of the arteries of the two sides, the right arteries being considerably thinner than the hypertrophied left arteries. In the case described by Ambrus14 (Table I, Case 1), the only example in which an artery arising near the innominate was not stenotic, the infant was only 6 days old, and the ductus was also patent. In all of the other cases in Table I, on the basis of descriptions or diagrams, we believe the ductus was functionally or anatomically closed. Right ventricular hypertrophy was present in all cases in Group 1, and in 2 (Cases 1 and 5) the left ventricle was also hypertrophied. Collaterals to the lung from bronchial or intercostal arteries were prominent in Cases 2, 4, 6 and 8. Adhesions between the right visceral and parietal pleura were noted in Cases 2,6 and 8. In our case there was extreme right atria1 enlargement and dilatation of the tricuspid ring, superior vena cava and azygos vein. We attributed this evidence of increased blood flow to the collateral circulation through the bronchial and intercostal arteries, with return of a portion of this blood to the right heart through the azygos system. This additional increase in the blood flow to the left lung might further the persistence of the fetal musculature and pulmonary hypertension on this side. Experimental demonstration of the importance of increased blood flow in the newborn period as a factor retarding the regression of the pulmonary musculature has been offered by Pool et al.‘5 in newborn dogs and calves. Grout 2: Table II summarizes some pathologic findings in 8 cases in which the right pulmonary artery arose from the ascending aorta. In 7 cases the precise origin of the anomolous artery was given. In 4, it arose from the right side of the aorta, in 2, from the posterior aspect and in only 1 case, from the left side of the aorta. The circumference of the right pulmonary artery was as large or larger than one would expect of a normal right pulmonary artery. In no case was there any narrowing of the right pulmonary artery from its origin in the aorta to the hilum of the right lung. Descriptions or photographs of the intrapulmonary arteries in most cases suggest that their similarity in both lungs indicates bilateral medial hypertrophy (or perTHE
AMERICAN
JOURNAL
OF CARDIOLOGY
Origin
of Right
Pulmonary
sistcnt fetal pattern) rather than normal vessels. It is interesting that in 1 case described by Pool and co-workers,l a pulmonary artery arising from the ascending aorta had the configuration of pulmonary artery. This finding supports their embryologic interpretation that when the right pulmonary artery arises from the ascending aorta, the bud has developed normally from the truncus but subsequently fails to migrate and so arises from the aorta. The Right Pulmonary Artery in Groufi 7: In Case 5 and in the present case, arterial tissue resembling ductus was present in the mid-portion Descriptions of of the right pulmonary artery. the microscopic structure of the right pulmonary artery were seldom given, so it is not possible to find out how often tissues of ductal origin were present in Group 1 cases. However, 2 cases support the theory that the brachiocephalic vessel represents, in part, right ductus arteriosus.’ A study of the gross descriptions of the right pulmonary artery of patients of different ages in group 1 suggested to us that narrowing of this artery might be progressive with age and might be correlated with closure of the left ductus arteriosus. We could find no evidence for the belief that closure of the right pulmonary artery in Group 1 cases begins in fetal life.5 In the youngest patient yet studied of this group (Case 1, Table I) the right pulmonary artery and the ductus were still patent. Surgical Implications: The relative hypertrophy or atrophy of the pulmonary vasculature of the left and right lungs may be of importance when surgical correction is considered. Successful repair by transplanting the anomalous right pulmonary artery from the aorta to the main pulmonary artery has been done in a case where the right pulmonary artery arose from the ascending aorta’ and the pulmonary arteries were equally developed on the two sides, but not when there was a stenotic segment. Whether or not the relatively atrophic condition of the media of the pulmonary arteries in the right lung compared to the left might complicate successful repair in Group 1 cases cannot be predicted, but the possibility should be kept in mind. We expect that operation may be the only treatment in this group of infants with pulmonary hypertension and congestive failure. SUMMARY
A case of isolated origin of the right pulmonary artery from the aorta is presented. Fifteen reVOLUME 19, MAY 1967
Artery from Aorta
747
ported autopsy cases in infants and children are reviewed and classified into two groups. In Group 1 the right pulmonary artery originated from or adjacent to the innominate artery, and there was usually stenosis or atresia of the right pulmonary artery. The llmg on the right side was poorly developed and the media of the pulmonary arteries normal to atrophic, with evidence of pulmonary hypertension on the left side. In Group 2 the right pulmonary artery arose from the ascending aorta, usually from the right or posterior aspect. Here, a wide communication was maintained between the pulmonary artery and aorta. In these cases there was bilateral medial hypertrophy of the intrapulmonary arteries. Certain features (x-ray, electrocardiographic and pathologic) that may permit separation of the two groups are discussed. ACKNOWLEDGMENTS The authors wish to thank Mrs. Elizabeth Cuzzort for the drawing (Fig. 3), Mrs. Elsie Chishoim for the histologic sections and Mr. Willy Kratel for the photomicrographs. REFERENCES 1. POOL, P. E., VOGEL, J. H. K. and BLOUNT, S. G. JR. Congenital unilateral absence of a pulmonary artery. The importance of flow in pulmonary hypertension. Am. J. Cardiol., 10: 706, 1962. 2. ANDERSON, R. C., CHAR, F. and ADAMS, P. JR. Proximal interruption of a pulmonary arch. (Absence of one pulmonary artery) : Case report and a new embryologic interpretation. Dis. Chest., 34: 73, 1958. 3. RUBIN, E. and STRAUSS,L. Congenital absence of the right pulmonary artery. Report of a case in a five month old infant, with suggestive evidence of unilateral pulmonary hypertension. Am. J. Cardiol., 6: 344, 1960. 4. GRIFFITHS, S. P., LEVINE, 0. R. and ANDERSEN, D. H. Aortic origin of the right pulmonary artery. Circulation, 25: 73, 1962. 5. WAGENVOORT,C. A., NEUFELD, H. N., BIRGE, R. F., CAFFREY, J. A. and EDWARDS,J. E. Origin of the right pulmonary artery from ascending aorta. Circulation, 23: 84, 1961. 6. ODELL, J. E. and SMITH, J. C. II. Right pulmonary artery arising from ascending aorta. Am. J. Dis. Child., 105: 87, 1963. 7. ARMER, R. M., SHUMACKER,H. B. and KLATTE, E. G. Origin of the right pulmonary artery from the ascending aorta. Report of a surgically corrected case. Circulation, 24: 662, 1961. 8. MADOFF, J. M., GAENSLER, E. A. and STRIEDER, J. W. Congenital absence of the right pulmonary artery. Diagnosis by angiography with cardiorespiratory studies. New England J. Med., 247: 149, 1952.
748
Kauffman,
Yao, Webber
9. STEINBERG, I.,
10.
11.
12.
13.
DOTTER, C. T. and LUCAS, D. S. Congenital absence of a main branch of the pulmonary artery. J.A.M.A., 152: 1216, 1953. MAIER, H. C. .-lbsence or hypoplasia of a pulmonary artery with anomalous systemic arteries to the lung. J. Thoracic. Surp., 28: 145, 1954. WYMAN, S. M. Congenital absence of a pulmonary artery: Its demonstration by roentgenography. Radiology, 62: 321, 1954. SCHNEIDERMAN,L. J. Isolated congenital absence A caution as to its of the right pulmonary artery: diagnosis and a proposal for its embryogenesis. Report of a case with review. Am. Heart J., 55: 772, 1958. FINDLAY, C. W., JR. and MAIER, H. C. Anomalies of pulmonary vessels and their surgical significance with review of literature. Surgery, 29: 604, 1951.
14. AMBRUS, G.
Congenital
absence of the right pul-
and Lynfield monary
artery with bleeding into the right lung.
J. Tech. Methods, 15: 103, 1936. 15. POOL, P. E., AVERILL, K. H. and VOGEL, H. K. Effect of ligation of left pulmonary artery at birth on maturation of pulmonary vascular bed. Med.
Thorac., 19: 362, 1962. 16. DUNNILL, M. S., and Ross, H. B.
Absent right pulmonary artery as an isolated congenital defect. Lancet, 2: 185, 1961. 17. DUSHANE, J. W. et al. Clinical-pathologic conference. Am. Heart J., 59: 782, 1960. 18. PORTER, D. D., CANENT, R. V. JR., SPACH, M. S. and BAYLEN, G. J. Origin of the right pulmonary artery from the ascending aorta. Unusual cineangiocardiographic and pathologic findings. Circulation, 27: 589, 1963. 19. MUDD, J. G., VALLEE, L. W. and RIBERBI, A. Origin of one pulmonary artery from the aorta. Am. Reo. Resp. Dir., 89: 255, 1964.
THE AMERICAN JOURNAL OF CARDIOLOGY
of the Right
Pulmonary
/
Artery
from the Aorta A Clinical-Pathologic
Study of Two Types Based on
Caliber of the Pulmonarv
J
Arterv* J
SHIRLEY L. KAUFF~IAN, M.D., ALICE C YAO, M.D., CAROLYN B. WEBBER, M.D. and JOSHUA LYNF~ELD, M.D., I;.A.c.c. Brooklb-n,
0
RIGIN of the right pulmonary artery from the aorta is a rare malformation of the arch system’ in which the right lung is perfused by the systemic and the left lung by the pulmonic circulation.2-4 Pulmonary hypertension may occurI,* and seems to be an important complication in those infants who die in the first year of life. The main anatomic types of isolated origin of the right pulmonary artery from the aorta seen in this group of infants are those in which the artery arises from the ascending aorta and those in which a brachiocephalic vessel supplies the right lung (Groups 7 and 9 of the classification of Pool et al.‘). The differences between these anatomic types are also reflected in the development of the pulmonary vasculature of the two lungs. In the case described by Anderson and colleagues,2 which they considered as proximal interruption of the pulmonary arch, the right pulmonary artery arose from the innominate and became obliterated, and the arteries in the right lung were thin-walled compared with the left lung. Rubin and Strauss3 and Wagenvoort and co-workersblater described somewhat similar cases in which the right pulmonary artery was narrowed or obliterated after its origin near the innominate ; here, was relative too, there atrophy of pulmonary arteries in the right lung and medial hypertrophy of arteries in the left lung. When the right pulmonary artery arose directly from the ascending aorta, without a
iVew York
narrowed -,egment, as in cases described by Griffiths et a1.,4 both lungs received excessive blood flow, and there was pathologic evidence of bilateral pulmonary hypertension. The explanation for the differences between these two forms of origin of the right pulmonary artery from the aorta is seen in the different embryologic origin of the two types.lb2 In tr-le absence of the right pulmonary artery, in which the right lung is supplied by a brachiocephalic vessel, Pool et al.’ considered that the vessel represents persistence of the ductal portion of the pulmonary arch. Wagenvoort and co-workers5 shared this interpretation and believed that the stenosis or atresia of the “right pulmonary artery” when it arises from a brachiocephalic vessel is due to the inherent tendency of ductal tissue to close. When the right pulmonary artery arises directly from the ascending aorta, it is considered a normal but displaced artery’ and as such would have no tendency to close. All of these studies suggest that it is largely the tendency of the artery to close that determines the size of the aortic-pulmonic connection, which, in turn, accounts for alterations in blood ~Iow’~~~~~~ and in the newborn, alterations in pulmonary vasculature. We present a case report of isolated origin of the right pulmonary artery from the aorta and a review of autopsy cases in infants which emphasizes the relationships of location of the right pulmonary artery, size of aortic-pulmonic communication and development of pulmonary
* From the Departments of Pathology and Pediatrics, State University of New York Downstate Medical Center, and Kings County Hospital, Brooklyn, N. Y. VOLUME
19,
MAY
1967
741
Kauffman, vasculature. may
Certain
help
to
clinical
differentiate
Yao,
featrrres*~” the
two
Webber
and
Lynfield
which
groups
are
also included. C.4s~
KEPORT
A 2 month old Negro female infant was admitted to Kings County Hospital on Sept. 20. 1964, because of difficulty in breathing. She was the product of a full term uncomplicated pregnancy, the first of an 18 year old mother. Birth weight was 5 lbs., 7 oz. No abnormalities were noted until four days prior to admission, when a cough and then respiratory distress developed. Physical Examination: The infant was well develWeight was oped and had mild, diffuse cyanosis. 8 Ibs., height 47 cm., pulse rate 152/min. and respiratory rate lOO/min. Blood pressure was 70/40 mm. Hg in the right arm and 80/50 in the right leg. Radial and femoral pulses were normal. The left precordium was prominent with a visible impulse, and the maximal palpable impulse was at the fourth intercostal space, 2 cm. beyond the left mid-clavicular line. The first heart sound was normal, and the second, single, and accentuated at the upper left sternal border. A grade 3-4/6 crescendo, almost pansystolic murmur was heard best along the lower left sternal border. Fine crepitant rales were heard at the left lung field posteriorly. The liver edge was palpable 4.5 cm. below the right costal margin. The nail beds were slightly cyanotic. Laboratory Data: Hemoglobin was 15 gm./lOO ml., white blood count 17,100 with 62yc neutrophils, 220/, lymphocytes, 14% monocytes and 2 eosiniphils. Roentgenograms of the chest (Fig. 1) showed moderate cardiomegaly, decreased vascular markings over the right lung field and increased markings over the left lung. The interspaces on the right were slightly narrower than on the left, and the right hemithorax
“I FIG. 2. atria1
Electrocardiogram and right ventricular
are
1.
Chest
narrowing
roentgenogram.
compared of the interspaces
hyperlucent
Lung
fields
with the left, on the right.
on
and
the
right
there
is
“5
“6
compatible with severe hypertrophy.
right
appeared smaller than the left. l‘he electrocardiogram (Fig. 2) showed a regular sinus rhythm with a rate of lbO/min., axis +150”, tall peaked P waves in lead II, S-T elevation in precordial leads and diphasic The electrocardiogram was interpreted as T in VI. indicating right axis deviation and severe right atria1 and ventricular hypertrophy. Hospital Course: The infant was placed in an oxygen croupette with mist and received digoxin and Mercuhydrin@ for heart failure and penicillin and Kantrex@ for possible pneumonia. She continued to have dyspnea and cyanosis, but from the fourth hospital day on showed slight but definite improvement. However, before any further diagnostic studies could be done, hematemesis with signs of intestinal obstruction developed, and the infant died. The diagnosis of absent right pulmonary artery with pcor collateral circulation was considered on the basis of chest roentgenogram. SUMMARY
FIG.
“2
OF
SIGNIFICANT
POSTMORTEM
FINDINGS
The heart (Fig. 3) lay in an oblique position with the right ventricle comprising the apex. The right atrium was extremely dilated and hypertrophied. It received a large superior vena cava, dilated coronary sinus and inferior vena cava. The foramen ovale was adequately covered by the septum primum but could be probed to a maximal diameter of 1.0 cm. The right ventricular cavity was dilated, and both the trabecular and compact myocardium were hypertrophied. A dilated pulmonary valve contained three normal cusps. The large main pulmonary artery, which was dilated above the valve, narrowed somewhat at the origin of a large, thickwalled ligamentum arteriosum and continued as the left pulmonary artery. The right pulmonary artery was absent. Four pulmonary veins entered a small left atrium. No abnormalities of the tricuspid, mitral, pulmonic: or aortic valve were present. The ventricular septum was intact. The valve and heart THE
AMERICANJOURNALOF
CARDIOLOGY
Origin
of Right
Pulmonary
Artery from Aorta
743
changed to a thin-walled vessel bvhirh graduall! dilated to a maximal circumference of 7 mm. at the hilum of the right lung where it gave off branches to three lobes. The remaining branches of the aorta were normal. ‘l-he right lung was also supplied by one large bronchial artery and intercostal arteries. The left lun,g was larger than the right and was dark red and firm. Prominent pleural vessels were seen over the right lung. A superficial gastric erosion was found on the lesser curvature of the stomach, and the upper 70 cm. of the jejunum was distended, purple and contained dark bloody fluid. MICROSCOPIC
EXAMINATION
Sections from all lobes of both lungs were examined. There was a striking difference between the two sides. Elastic and muscular pulmonary arteries of the left lung showed severe medial hypertrophy and elastosis (Fig. 4A), while those of the right lung were extremely thin walled (Fig. 4B). Many arteries of the right lung had only a thin rim of muscularis between the internal and external limiting membranes, and in others no muscularis was identified. The mean ratio of media to total diameter of arteries less than 100 p was 15.7 per cent in the left lung and 4.1 in the right lung. The mean ratio of arteries of 8 matched control infants without heart or lung disease was 4.6yo f 1.6. Sections of the main pulmonary artery showed the expected fetal elastica pattern and moderate intimal thickening. Sections taken at the origin of the anomalous right pulmonary artery showed parallel bands of elastic tissue continuous from the aorta into this At the narrow mid-portion of the artery (Fig. vessel. 5A), the elastica was fragmented, and the arrangement of bundles of smooth muscle was similar to that found in the left ligamentum arteriosum. There was no intimal thickening. Distally, the vessel resembled the intramural pulmonary artery (Fig. 5B). The left Lungs:
Fro. i.
I)r.Iwina or hrart. lungs and great vessels shows the anomalcrus right pulmonary artery arising just proximal to the innominate artery. It enters the hilum at the arrow. The right pulmonary artery narrows to 3 mm. in circumference at the point whve it is crossed by a prominent azygos vein. The right lung is smaller than the left. The right atrium and right ventricle are dilated and hypertrophied. The ductus arteriosus, which appears large externally, is closed.
measurements were as follows: tricuspid 6.0 cm., pulmonary 2.5 cm., mitral 3.0 cm. and aortic 2.0 cm. in circumference; the right ventricle and left ventricle each measured 5 mm. in thickness. The jirst aortic branch was an artq to the right lung which arose 2.5 cm. distal to the aortic valve immediately inferior to the innominate artery (Fig. 3). At its origin the right pulmonary artery measured 6 mm. in circumference and was thick-walled. It narrowed abruptly to 3 mm. in circumference where it was crossed by the azygos vein. Past the point of crossing, the right anomalous pulmonary artery abruptly
A
B
FIG. 4. A, a thick-walled pulmonary artery representative of those in the left lung shows medial hypertrophy and elastosis. (Verhoeff-Van Gieson X 250.) B, typical thin-walled intrapulmonary artery in the right lung; many other small arteries contained no recognizable media. (Verhoeff-Van Gieson X 250.) VOLUME
19.
MAY
1967
744
Kauffman,
Yao, Webber
and Lynfield
n
A
FIG. 5. A, longitudinal section of the right pulmonary artery along the region of narrowing. The lumen of the artery is to the right. Note thick, fragmented elastica and arrangement of muscular-is resembling ductus arteriosus. (Verhoeff-Van Gieson X 70.) B, right pulmonary artery distal to narrowed segment shows a normal configuration of elastica for this age. (Verhoeff-Van Gieson X 70.)
ductus arteriosus was closed and showed intimal liferation and zones of calcification (Fig. 6).
REVIEW
FIG. 6. Cross section of (Verhoeff-Van artel riosum.
normal Gieson
X
left ligamentur n 15.)
OF
pro-
THE LITERATURE AND DISCUSSION
Tables I and II summarize 16 autopsy cases of isolated origin of the right pulmonary artery from the aorta in children. References to many interesting cases in earlier literature which involve both adults and children in whom a diagnosis was made clinically can be found elsewhere.6~s~10-13 We excluded these cases because they contained too few details for analysis. Table I summarizes the major findings in patients whose right pulmonary artery arose in the vicinity of the innominate artery (Group l), and Table II summarizes the cases of those patients whose right pulmonary artery arose from the ascending aorta (Group 2). There were 8 patients in each group, and 6 in each group died before the age of 5 months. THE
AMERICAN
JOURNAL
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Origin
of Right
Pulmonary
Artery
TABLE
Origin of the Right
Age at Death
C:ase No. Reference 1ip
SeX
6 days
22
Pulmonary
I
Artery from the Aorta (Vicinity Vascular Markings Roentgenogram
ECG
F
.
14 mo.
M
RAD RAE RVH
L. > R.
745
from Aorta
of the Innominate
---------Autopsy Small Pulmonary :\rteries I,. R.
-----
Heart LVH RVH
”
‘.
RVH
H
D
.Irtery)
(Group
1)
Findings-----------~ Right Pulmonary Artery Origin Circ.* Innom.
0 ‘)5 cm.
Innom.
Oblit.
312
6 wk.
M
RVH
L. > R.
RVH
Prox. to innom.
0.2 cm.
43
4 mo.
M
RAD RVH
N
RVH
H
D
Prox. to innom.
Oblit.
56
3 wk.
F
RVH LVH
H
D
Base of innom.
“Narrow”
66
14 mo.
M
.. .
RAH RVH
;,
?
Innom.
“Pin-point”
7”
2 mo.
M
RAH RVH
L. > R.
RAH RVH
H
N
Base of innom.
“Quite small”
8
2 mo.
F
RAE RVH
L. > R.
RAH RVH
H
D
Base of innom.
0.3 cm.
(present case)
N
_.
_,
* Circumference of narrowest portion. LVH = left ventricular hypertrophy; L. = left; R. = right; RVH = right ventricular hypertrophy; Innom. = H = hypertrophied; D = dilated; innominate artery; RAD = right axis deviation; RAE = right axis elevation; Oblit. = obliterated; Prox. = proximal; RAH = right atria1 hypertrophy; N = normal. TABLE
Origin of the Right
Pulmonary
Vascular Markings Roentgenogram
II
Artery from the Ascending Y-Autopsy
Sex
913*
4 mo.
F
NAD
Increased
RVH LVH
10’7
2 mo.
F
RAE RVH LVH
Increased
LVH LAD LVD
114
6’/2 mo.
F
NAD LVH RVH Tall P
Prominent
RVH LVH
H
EGG
Heart
2)
Findings------~ Small Pulmonary Right Pulmonary Arteries Artery L. Origin Circ. R.
Age at Death
Case No.
Aorta (Group
“No difference”
H
Ductus
Aorta (L.) Aorta (R.)
2.7 cm.
Cl
l.Ocm.
0
Aorta
3.7 cm.
Cl
(post.)
124
33 mo.
M
RAD RVH Tall P
Prominent
RVH LVH
H
H
Aorta (R.)
3.5 cm.
Cl
13i8
25 days
M
RVH
Prominent R. > L.
RVH
“N”
“N”
1.3cm.
0
146
2 mo.
M
RAH RVH
Increased R. > L.
RVH RAH
“N”
“N”
Aorta (R.) Aorta
0.7 cm.
Cl
156
2 mo.
F
LVH
Increased R. > L.
LVH
“Large”
0
16’9
14 wk.
M
RVH
Increased
“Large”
0
.
“N”
H(F)
“Similar”
Aorta (R.) Aorta (post.)
* Also reported as Maier case 310 and Griffiths case 1.4 Abbreviations same as Group 1; in addition: 0 = open; posterior. VOI LIME
19:
MAY
1967
Cl = closed (anatomically
or physiologically)
; post. =
Kauffman, CLINICAL
Yao,
Webber
FEATURES
In both groups, respiratory distress, cyanosis, pulmonary hypertension and intractable congestive heart failure developed in the infants in the first weeks or months of life. Chest roentgenograms showed cardiomegaly in patients of both groups, but often differences were noted in pulmonary vascular markings.8-11 In Group 1 the vasculature of the right lung was diminished, while that of the left was normal or increased (Cases 2, 3, 7 and 8). Since the blood flow to the right lung is decreased in cases of stenosis or atresia of the right pulmonary artery, the right hemithorax, as well as the right lung, may be smaller than the left (Cases 2, 4 and 8). In Group 2 cases, by contrast, the pulmonary vasculature was often increased or prominent on both sides, or the right lung had increased vascular markings. The right and left lungs in Group 2 cases were the same size. Review of available electrocardiograms showed a constancy of signs of right atria1 and right ventricular hypertrophy in Group 1 cases. In patients whose pulmonary artery arose from the ascending aorta (Group 2), there were variable patterns from pure right to left ventricular or biventricular hypertrophy. These differences reflect the different hemodynamics in the two groups. In patients of both groups the left lung received the total output of the right ventricle under systemic pressure. This increased flow and pressure, probably accompanied by vasoconstriction,3 may be important in delaying the normal regression of the fetal pattern of the muscular arteries in these small infants. In Group 2, where a wide communication between the aorta and right pulmonary artery was maintained, the right lung also received blood under systemic pressure, and left ventricular hypertrophy eventually ensued. In addition, in some of these patients the ductus arteriosus was patent. PATHOLOGIC
FEATURES
Group 9: In the 8 patients whose right pulmonary artery arose from or adjacent to the innominate artery (Table I), 7 showed a stenotic or atretic segment in the pulmonary artery. Often the artery was funnel-shaped, with the maximal narrowing in the center and flaring on either side. The exact caliber of the stenotic artery was not given in most cases, but the vessel was extremely narrow and in 2 instances was atretic. It is interesting that the youngest
and
Lynfield
infants had patent vessels, while the oldest had vessels with pinpoint (Case 6) or atretic lumens (Cases 2 and 4). Though the small pulmonary arteries were not always completely described, it was possible in many cases to recognize the differences in media of the arteries of the two sides, the right arteries being considerably thinner than the hypertrophied left arteries. In the case described by Ambrus14 (Table I, Case 1), the only example in which an artery arising near the innominate was not stenotic, the infant was only 6 days old, and the ductus was also patent. In all of the other cases in Table I, on the basis of descriptions or diagrams, we believe the ductus was functionally or anatomically closed. Right ventricular hypertrophy was present in all cases in Group 1, and in 2 (Cases 1 and 5) the left ventricle was also hypertrophied. Collaterals to the lung from bronchial or intercostal arteries were prominent in Cases 2, 4, 6 and 8. Adhesions between the right visceral and parietal pleura were noted in Cases 2,6 and 8. In our case there was extreme right atria1 enlargement and dilatation of the tricuspid ring, superior vena cava and azygos vein. We attributed this evidence of increased blood flow to the collateral circulation through the bronchial and intercostal arteries, with return of a portion of this blood to the right heart through the azygos system. This additional increase in the blood flow to the left lung might further the persistence of the fetal musculature and pulmonary hypertension on this side. Experimental demonstration of the importance of increased blood flow in the newborn period as a factor retarding the regression of the pulmonary musculature has been offered by Pool et al.‘5 in newborn dogs and calves. Grout 2: Table II summarizes some pathologic findings in 8 cases in which the right pulmonary artery arose from the ascending aorta. In 7 cases the precise origin of the anomolous artery was given. In 4, it arose from the right side of the aorta, in 2, from the posterior aspect and in only 1 case, from the left side of the aorta. The circumference of the right pulmonary artery was as large or larger than one would expect of a normal right pulmonary artery. In no case was there any narrowing of the right pulmonary artery from its origin in the aorta to the hilum of the right lung. Descriptions or photographs of the intrapulmonary arteries in most cases suggest that their similarity in both lungs indicates bilateral medial hypertrophy (or perTHE
AMERICAN
JOURNAL
OF CARDIOLOGY
Origin
of Right
Pulmonary
sistcnt fetal pattern) rather than normal vessels. It is interesting that in 1 case described by Pool and co-workers,l a pulmonary artery arising from the ascending aorta had the configuration of pulmonary artery. This finding supports their embryologic interpretation that when the right pulmonary artery arises from the ascending aorta, the bud has developed normally from the truncus but subsequently fails to migrate and so arises from the aorta. The Right Pulmonary Artery in Groufi 7: In Case 5 and in the present case, arterial tissue resembling ductus was present in the mid-portion Descriptions of of the right pulmonary artery. the microscopic structure of the right pulmonary artery were seldom given, so it is not possible to find out how often tissues of ductal origin were present in Group 1 cases. However, 2 cases support the theory that the brachiocephalic vessel represents, in part, right ductus arteriosus.’ A study of the gross descriptions of the right pulmonary artery of patients of different ages in group 1 suggested to us that narrowing of this artery might be progressive with age and might be correlated with closure of the left ductus arteriosus. We could find no evidence for the belief that closure of the right pulmonary artery in Group 1 cases begins in fetal life.5 In the youngest patient yet studied of this group (Case 1, Table I) the right pulmonary artery and the ductus were still patent. Surgical Implications: The relative hypertrophy or atrophy of the pulmonary vasculature of the left and right lungs may be of importance when surgical correction is considered. Successful repair by transplanting the anomalous right pulmonary artery from the aorta to the main pulmonary artery has been done in a case where the right pulmonary artery arose from the ascending aorta’ and the pulmonary arteries were equally developed on the two sides, but not when there was a stenotic segment. Whether or not the relatively atrophic condition of the media of the pulmonary arteries in the right lung compared to the left might complicate successful repair in Group 1 cases cannot be predicted, but the possibility should be kept in mind. We expect that operation may be the only treatment in this group of infants with pulmonary hypertension and congestive failure. SUMMARY
A case of isolated origin of the right pulmonary artery from the aorta is presented. Fifteen reVOLUME 19, MAY 1967
Artery from Aorta
747
ported autopsy cases in infants and children are reviewed and classified into two groups. In Group 1 the right pulmonary artery originated from or adjacent to the innominate artery, and there was usually stenosis or atresia of the right pulmonary artery. The llmg on the right side was poorly developed and the media of the pulmonary arteries normal to atrophic, with evidence of pulmonary hypertension on the left side. In Group 2 the right pulmonary artery arose from the ascending aorta, usually from the right or posterior aspect. Here, a wide communication was maintained between the pulmonary artery and aorta. In these cases there was bilateral medial hypertrophy of the intrapulmonary arteries. Certain features (x-ray, electrocardiographic and pathologic) that may permit separation of the two groups are discussed. ACKNOWLEDGMENTS The authors wish to thank Mrs. Elizabeth Cuzzort for the drawing (Fig. 3), Mrs. Elsie Chishoim for the histologic sections and Mr. Willy Kratel for the photomicrographs. REFERENCES 1. POOL, P. E., VOGEL, J. H. K. and BLOUNT, S. G. JR. Congenital unilateral absence of a pulmonary artery. The importance of flow in pulmonary hypertension. Am. J. Cardiol., 10: 706, 1962. 2. ANDERSON, R. C., CHAR, F. and ADAMS, P. JR. Proximal interruption of a pulmonary arch. (Absence of one pulmonary artery) : Case report and a new embryologic interpretation. Dis. Chest., 34: 73, 1958. 3. RUBIN, E. and STRAUSS,L. Congenital absence of the right pulmonary artery. Report of a case in a five month old infant, with suggestive evidence of unilateral pulmonary hypertension. Am. J. Cardiol., 6: 344, 1960. 4. GRIFFITHS, S. P., LEVINE, 0. R. and ANDERSEN, D. H. Aortic origin of the right pulmonary artery. Circulation, 25: 73, 1962. 5. WAGENVOORT,C. A., NEUFELD, H. N., BIRGE, R. F., CAFFREY, J. A. and EDWARDS,J. E. Origin of the right pulmonary artery from ascending aorta. Circulation, 23: 84, 1961. 6. ODELL, J. E. and SMITH, J. C. II. Right pulmonary artery arising from ascending aorta. Am. J. Dis. Child., 105: 87, 1963. 7. ARMER, R. M., SHUMACKER,H. B. and KLATTE, E. G. Origin of the right pulmonary artery from the ascending aorta. Report of a surgically corrected case. Circulation, 24: 662, 1961. 8. MADOFF, J. M., GAENSLER, E. A. and STRIEDER, J. W. Congenital absence of the right pulmonary artery. Diagnosis by angiography with cardiorespiratory studies. New England J. Med., 247: 149, 1952.
748
Kauffman,
Yao, Webber
9. STEINBERG, I.,
10.
11.
12.
13.
DOTTER, C. T. and LUCAS, D. S. Congenital absence of a main branch of the pulmonary artery. J.A.M.A., 152: 1216, 1953. MAIER, H. C. .-lbsence or hypoplasia of a pulmonary artery with anomalous systemic arteries to the lung. J. Thoracic. Surp., 28: 145, 1954. WYMAN, S. M. Congenital absence of a pulmonary artery: Its demonstration by roentgenography. Radiology, 62: 321, 1954. SCHNEIDERMAN,L. J. Isolated congenital absence A caution as to its of the right pulmonary artery: diagnosis and a proposal for its embryogenesis. Report of a case with review. Am. Heart J., 55: 772, 1958. FINDLAY, C. W., JR. and MAIER, H. C. Anomalies of pulmonary vessels and their surgical significance with review of literature. Surgery, 29: 604, 1951.
14. AMBRUS, G.
Congenital
absence of the right pul-
and Lynfield monary
artery with bleeding into the right lung.
J. Tech. Methods, 15: 103, 1936. 15. POOL, P. E., AVERILL, K. H. and VOGEL, H. K. Effect of ligation of left pulmonary artery at birth on maturation of pulmonary vascular bed. Med.
Thorac., 19: 362, 1962. 16. DUNNILL, M. S., and Ross, H. B.
Absent right pulmonary artery as an isolated congenital defect. Lancet, 2: 185, 1961. 17. DUSHANE, J. W. et al. Clinical-pathologic conference. Am. Heart J., 59: 782, 1960. 18. PORTER, D. D., CANENT, R. V. JR., SPACH, M. S. and BAYLEN, G. J. Origin of the right pulmonary artery from the ascending aorta. Unusual cineangiocardiographic and pathologic findings. Circulation, 27: 589, 1963. 19. MUDD, J. G., VALLEE, L. W. and RIBERBI, A. Origin of one pulmonary artery from the aorta. Am. Reo. Resp. Dir., 89: 255, 1964.
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