Download cor biloculare with transposition of the great cardiac vessels and

COR BILOCULARE WITH TRANSPOSITION OF T H E GREAT CARDIAC
VESSELS AND ATRESIA OF T H E PULMONARY ARTERY.
PHYLOGENETIC AND ONTOGENETIC INTERPRETATION
J. I. ROSSMAN*
From the Henry Baird Favill Laboratory of St. Luke's Hospital, Chicago, Illinois
Cor triloculare, or complete absence of both the auricular and ventricular
septums, is a rare congenital cardiac anomaly. In all, thirty-seven hearts with
this malformation have been reported. However, a wide range in the extent of
septal development is described in the various reports and Maud E. Abbott 1 ,
in her Atlas, published in 1936 accepts only fourteen. Septal development in
the heart of this report is sufficiently elementary to classify the anomaly definitely as a cor biloculare. In addition, there is complete transposition of the
great cardiac vessels and atresia of the pulmonary artery. No description of
an exactly similar combination of defects has been recorded, though similar
hearts with minor differences have been described by Wood and William2,
Kugel3, Shapiro4, and Lightner5. In the older literature, as reviewed by Abbott
in Osier's Modern Medicine6, no similar description is recorded. Numerous
additional somatic deformities add interest to the description of this heart.
CASE REPORTS
A white male infant, aged nine and a half months, was born as a breech presentation at
St. Luke's Hospital, Chicago, on October 6, 1940. The past history and physical examination of the mother, a primipara, aged 22, were not significant. After delivery the infant
remained cyanotic. The cervical spine was short, the head seemed to rest directly on the
shoulders and there was an angular kyphosis and a flail joint at the junction of the thoracic
and lumbar spines. There was a spastic paraplegia of both lower extremities. Examination of the heart was entirely negative though the presence of congenital heart disease was
suspected. The child continued to have increasingly severe attacks of cyanosis and
dyspnea and during one of these, he died. .
Autopsy. Besides the congenital cardiac anomaly the following somatic anomalies were
also present: moderate spina bifida of the second, third, fourth, fifth, and sixth cervical
vertebrae; maldevelopment of the last thoracic and upper two lumbar vertebrae with a
loose fibrous connection between them; incomplete rotation of the large and small intestine;
situs inversus of the stomach, duodenum, foramen epiploicum, pancreas, liver, and gall
bladder; agenesis of the spleen; an accessory lobe of the left lung; and bilateral indirect
inguinal hernias with the caecum and the appendix in the right hernial sac.
Heart. The heart, enclosed in a pericardial sac, was triangular, lying in the center of the
chest. From its base, one large arterial trunk arose and curved to the left (fig. la). Three
large vessels arose normally from the arch and extended to the neck. The heart was 5.5
cm. transversely at the base, 5.2 cm. along the right border and 4.4 cm. along the left border.
It was 3 cm. thick at the base and 2 cm. thick at the apex. There was a large patent ductus
arteriosus (fig. lb) which arose 3 cm. from the root of the aorta, extended postero-inferiorly
1.4 cm. and then divided into a narrow branch which passed to the left lung (fig. Id) and a
larger, thin-walled branch (fig. lc) 1 cm. in diameter, which extended to the right lung.
Extending from the latter branch, in the position of the pulmonary artery, was a thin fibrous
* The John Jay Borland Fellow.
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COR BILOCULARB
535
cord, 2.5 cm. long and 0.1 cm. in diameter (fig. l e ) . T h e cardiac end was lost in t h e tissues
about the posterior surface of the a o r t a . The heart consisted of a single large auricle which
led through a common atrioventricular orifice into a large common ventricle which in t u r n
emptied through the large anteriorly placed aorta. The auricle was dilated, its maximum
internal diameter being 7.5 cm. I t was crossed by a muscular band 1.5 cm. long and 0.3 cm.
in diameter which extended diagonally from the right upper region of the posterior auricular
wall to the midpoint of the anterior wall inferiorly (fig. 2a). The right upper and posterior
corner of the auricle was widened and received both the superior and inferior vena cavas
through a common opening (fig. 2b). There was an ill-defined crista terminalis (fig. 2c),
and midway along this opened the coronary sinus, guarded by an elementary Thebesian
F I G . 1. DIAGRAMMATIC SKETCH ILLUSTRATING THE V E S S E L S AT THE B A S E OF THE H E A R T
(a) Aorta, (b) ductus arteriosus, (d) branch to the left lung, (c) branch to t h e right lung,
and (e) atretic pulmonary artery.
valve (fig. 2d). Two small pulmonary veins (fig. 2e) opened separately into the left upper
and posterior corner of the auricle.
The atrioventricular orifice (fig. 2f) was 8.5 cm. in circumference and was guarded by
four coarsely wrinkled nodular fibrous tissue leaflets. The anterior leaflet was large (fig.
2g). I t was 1.4 cm. long and 3.5 cm. wide and was attached to each lateral wall by a group
of papillary muscles. The other leaflets were smaller and indistinctly separated. T h e left
was attached to a well-defined group of papillary muscles b u t the right and the posterior
leaflets were attached to several chordae tendinae whose corresponding papillary muscles
were buried in the left ventricular wall.
The wall of the ventricle was coarsely trabeculated (fig. 2, 3). Beginning a t the apex
a n d extending along the posterior wall in the midline was a thick muscular ridge, 1 cm. high
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J. I. ROSSMAN
and 2 cm. long, occupying the position of the posterior portion of the true interventricular
septum (fig. 2h, 3b). There were two other ill-defined muscular ridges immediately proximal to the aortic ring. One, in front of and to the left of the aortic orifice, was 3 cm. long
and 2 cm. high and extended across the roof and slightly down the anterior wall of the ventricle (fig. 3d). The other ridge, posterior and to the right of the aorta, was about 2.5 cm.
long and 2 cm. high (fig. 3c) and extended across the roof and down the right wall of the
FIG. 2. SKETCH OF THE COMMON AURICLE AND VENTRICLE VIEWED PROM BEHIND
(a) Sagittal muscular bar representing the auricular septum, (b) common entry for the
superior and inferior vena cava, (c) crista terminalis, (d) entry of the coronary sinus with
the elementary Thebesian valve, (e) left and right pulmonary veins, (f) common auriculoventricular opening, (g) large anterior atrioventricular leaflets, and (h) rudimentary
interventricular septum.
ventricle. The two ridges had a common commissure posterior to the aorta and from
behind this arose the large anterior leaflet of the atrioventricular orifice (fig. 3a). The
first two of these three ridges together formed an elementary interventricular septum which
in no way impeded the flow of blood. The average thickness of the ventricular wall was
0.9 cm. The aortic ring (fig. 3) was situated anteriorly and slightly to the right. The
circumference was 3.5 cm. There were three thin, tough, well-formed aortic leaflets, an
anterior, a left and a right posterior, and patent coronary vessels arose from behind the
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COR BILOCULAHE
F I G . 6. SKETCH OF THE V E N T R I C L E
FROM IN
FRONT
(a) Anterior atrioventricular leaflet, (b) vestigial interventricular septum, (c) posterior preaortic muscle mass (vestigial bulbo-atrial fold), (d) anterior preaortic muscle
mass (crista supraventricularis), (e) tricuspid aortic valve with left and right posterior
coronary-bearing cusps, (f) groove on the posterior aspect of the aorta, and (g) ductus
arteriosus.
Normal
F I G . 4. DIAGRAMMATIC SKETCH, COMPARED WITH THE N O R M A L , SHOWING D E T O R S I O N OF THE
AORTIC C U S P S AND TRANSPOSITION OF THE CORONARY A R T E R I E S
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J. I. ROSSMAN
latter two cusps. The lining of the aorta was smooth. Extending from the posterior commissure of the aortic valve along the posterior aortic wall for a distance of 3 cm. was an illdefined groove (fig. 3f) and at its distal end was the mouth of the patent ductus arteriosus.
The coronary arteries (fig. 4) were well-developed. The left coronary artery extended
from the left posterior aortic cusp and was mainly spent in several branches to the left
anterior surface of the heart. A small branch continued to the left to join a branch of the
right coronary artery. The right coronary artery arose from the right posterior aortic
cusp and supplied the right posterior surface of the heart. Histological examinations revealed no evidence of inflammation of the myocardium or endocardium.
Anatomical diagnosis. Transposition of the large vessels at the base of the heart; transposition of the aortic cusps and the coronary arteries; atresia of the pulmonary artery;
patent dctus arteriosus; vestigial interauricular septum; anomalous entry of the inferior
and superior vena cavas and the pulmonary veins; elementary crista terminalis and
Thebesian valve; common atrioventricular orifice; rudimentary interventricular septum;
hypertrophy of the crista supraventricularis and the bulbo-atrial ridge; situs inversus of the
stomach, duodenum, pancreas, foramen epiploicum, liver and gall bladder; incomplete
rotation of the large and small bowel; agenesis of the spleen; bilateral indirect inguinal
hernias; malformation of the spine; accessory lobe of the left lung.
DISCUSSION
This is essentially a primitive two-chambered heart with transposition of the
great cardiac vessels and atresia of the pulmonary artery. To interpret this
complicated anomaly recourse was had to a theory which related this heart to
those of lower forms of life. Maud Abbott, in her Atlas, stated that anomalies
of this type could not be explained on an embryological basis. In 1937, however, Lev and Saphir7 proposed an ontogenetic explanation for transposition
of the great cardiac vessels based on earlier work of Pernkopf and Wirtinger8.
The latter pointed out that at one stage in ontogeny there is an excessive spiraling of the bulbar septums. Normal relationships are established by a corrective
partial untwisting at either end of the bulbar septum. Lev and Saphir emphasized that this process is intimately dependent upon normal absorption of the
bulbus and showed how transposition of the great vessels could arise if absorption were faulty. In 1923, Spitzer9 advanced the most satisfactory theory concerning the role of phylogeny in the formation of congenital cardiac defects.
Though there is much to be said for Lev and Saphir's theory, yet in this particular case morphology seems to be interpreted best by reference to Spitzer's
work. Reference is made here only to the essential portions of the latter's
theory. A more thorough interpretation can be found in Harris and Farber's 10 excellent paper.
After studying a large series of hearts from lower forms of life, Spitzer stated
that with the advent of the pulmonary circulation the simple tube-like heart
of gill breathing organisms, with its tandem arrangement of chambers, undergoes a division into a four-chambered structure with left and right halves.
Concomitantly, the bulbar end of the heart undergoes a clockwise torsion of
180 degrees to establish a mechanism whereby aerated blood from the right half
of the heart can pass into the left half for further systemic distribution. Spitzer
postulated failure of complete torsion or, conversely, some degree of detorsion
at the bulbar end of the heart as the cause of those cardiac anomalies having
COR BILOCULAEE
539
some degree of transposition of the great cardiac vessels. Associated frequently
are anomalies of the aortic and pulmonary cusps and the coronary arteries.
The septums of the heart, subject to unusual influences, may develop in unusual
ways and vestigial structures, glossed over in ontogeny, may remain as functioning structures explicable only by reference to the hearts of more primitive organisms. Of these vestigial structures, the most important is the primitive
right aorta, seen best in the hearts of reptiles where it serves to deflect a portion
of the blood from the right ventricle of the heart into the systemic circulation
and away from the yet immature pulmonary system. Two vestigial septums
that hypertrophy and assume important roles are the crista supraventricularis
and the bulboatrial ledge. The crista supraventricularis is the prolongation of
the septum between the anteriorly placed pulmonary artery and the posteriorly
FIG.
5. DIAGRAMS
ILLUSTRATING THE FORMATION AND THE V A R I O U S
T R A N S P O S I T I O N OF T H E G R E A T CARDIAC V E S S E L S
DEGREES
OF
P) the pulmonary artery, A) t h e aorta, (R.A.) t h e right aorta, (L.A) the left aorta,
(a) t h e normal arrangement of the great cardiac vessels, (b) conditions with a slight degree
of detorsion, (c) conditions with further detorsion indicating how t h e right aorta assumes
the functioning role while the left aorta atrophies, (d) complete transposition of the great
cardiac vessels.
placed aortas in the reptilian heart and extends as an arch across the roof of the
right ventricle. The bulbo-atrial ledge is a portion of the original fold between
the descending and ascending portion of the primitive ventricular loop and appears as a ridge situated anterior to the tricuspid valve and posterior to the
right aorta in very primitive hearts.
All degrees of detorsion can occur from a slight untwisting of the aorta about
the pulmonary artery to a complete 180 degree untwisting in which the normal
relationship of aorta and pulmonary artery are reversed. The pertinent features of this process are illustrated in figure 5. The normal relationship of
pulmonary artery to aorta are indicated in figure 5a with the position of right
aorta of reptiles also indicated. With a slight degree of counter-clockwise untwisting the left aorta fuses with the right aorta which reopens. The pulmonary
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J. I. ROSSMAN
artery, now more anteriorly situated, is stenotic and frequently bicuspid. The
large aorta overrides a ventricular septal defect. This combination of anomalies
constitutes the tetralogy of Fallot. With further untwisting the left aorta
atrophies and only the primitive right aorta remains (fig. 5c). Complete 180
degrees detorsion is shown in the last diagram of the series (fig. 5d) in which the
vessels are transposed. Spitzer pointed out that there is thus no true transposition but rather a substitution of one vessel for another.
Of the great number of anomalies which can occur in this process of detorsion,
Spitzer recognized four main types. One of these, Type 3 or "crossed transposition" type is indicated diagramatically in figure 6a. The large cardiac ves-
F I G . 6. DIAGRAMS ILLUSTRATING THE STRUCTURE OF (a) S P I T Z E R ' S CROSSED T R A N S P O S I T I O N
OR T Y P E I I I H E A R T AND (b) THE H E A R T OF T H I S R E P O R T . T H E STRUCTURES A R E P R O JECTED ON THE VENTRICULAR B A S E W H I C H I S V I E W E D FROM ABOVE AND P O S T E R I O R L Y .
(After Harris and Farber, after Spitzer)
(1) Pulmonary artery, (2) aorta, (3) mitral valve, (4) tricuspid valve, (5) crista supraventricularis, (6) anterior portion of t h e interventricular septum, (7) posterior portion of
t h e interventricular septum, (8) site of the obliterated left ventricular aorta, (9) site of
t h e undeveloped true interventricular septum, (10) bulbo-atrial ledge, and (11) common
atrioventricular orifice.
sels are completely transposed and the pulmonary artery is stenotic and bicuspid. Only the posterior portion of the true interventricular septum remains
and the crista supraventricularis, between the aorta and pulmonary artery, has
hypertrophied and has rotated anteriorly to form a false anterior portion of the
interventricular septum. The bulbo-atrial ledge, between the tricuspid valve
and the aorta also hypertrophies. The pulmonary artery thus arises from the
left ventricle and the aorta from the right ventricle.
Spitzer then stated that if the crista supraventricularis is not properly situated to meet the posterior portion of the interventricular septum, neither of
these structures will develop and only a rudimentary septum results whereby
a cor biloculare or a heart with one ventricle and two atria is formed. This
COE BILOCDLARE
541
would seem to be the interpretation of the anomalous heart of my'report. It
is depicted diagramatically in figure 6b. Structurally it is closely related to
figure 6a. The great vessels are completely transposed and the two muscular
ridges, described above, situated proximal to the aortic orifice, are the crista
supraventricularis and the bulbo-atrial ledge. The muscular ridge at the apex
of the ventricle and extending up the posterior wall is the posterior portion of
the true interventricular septum. The common atrioventricular orifice overrides
the large interventricular defect. The explanation of the atresia of the pulmonary artery is not clear. Perhaps the large muscle bundle assumed here to be the
crista supraventricularis is really formed by a fusion of the crista and the anterior portion of the true interventricular septum. The pulmonary artery situated
between them is then constricted and becomes atretic. The atresia could also
be explained by assuming that the aorta attained an early dominant role in
transporting the blood while the pulmonary artery grew progressively smaller.
The concept of 180 degree detorsion defect is further substantiated by the
position of the aortic cusps and the coronary arteries (fig. 4). In place of the
normal arrangement in which there are a posterior non-coronary and a left and
a right anterior coronary bearing cusps, there are in this heart an anterior noncoronary and a left and a right posterior coronary bearing cusp. The left
coronary artery thus arises from what was destined to be the right coronary
bearing cusp and the right coronary artery from what was destined to be the
left coronary bearing cusp. They are completely transposed.
Although the primary defect in this heart was incomplete rotation of the
bulbar region, other abnormal features of the heart similarly reflect a lack of
inherent growth vitality and are best interpreted in terms of embryology. The
definitive auricular septum is formed by the fusion of the primitive overlapping
septum primum and septum secundum. At one stage, about the fifth week of
intrauterine life, the septum primum is represented by a sagittally placed muscular bar covered by the septum secundum. Development in this heart stopped
at this stage. The septum secundum failed to develop. Other primitive features of the auricle are the common opening for the superior and inferior vena
cavas, the presence of only two pulmonary veins in place of the four normally
present, and the elementary crista terminalis. The common atrioventricular
orifice is guarded by four leaflets indicative of their origin from the four endocardial cushions which line the atrioventricular orifice of the early fetus. The
vestigial interventricular septum has attained the height of the septum in a
five-week old fetus. The ductus arteriosus has remained patent and together
with the branches of the original pulmonary artery serves as the artery to the
lungs. The branch to the left lung is small but the branch to the right lung has
retained the large thin-walled caliber of the original pulmonary artery.
SUMMARY
The clinical record and autopsy findings of an infant, aged nine months, are
described. Amongst many other somatic anomalies there was a marked congenital cardiac malformation characterized by cor biloculare, complete trans-
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J. I. ROSSMAN
position of the great cardiac vessels, and atresia of the pulmonary artery. An
explanation for the malformation is offered on the basis of interruptions in
phylogenetic and ontogenetic development.
REFERENCES
(1) ABBOTT, M. E . : Atlas of Congenital
Cardiac Disease. New York, American H e a r t Association, 1936.
(2) W O O D , R.
"
(3)
(4)
(5)
(6)
H.,
AND W I L L I A M S , G.
Philadelphia, Lea and Febiger, 1927,
vol. 4, p . 720.
(7) L E V , M., AND SAPHIR, O.: Transposi-
tion of large vessels.
Methods, 19: 148, 1939.
A.:
Primitive human hearts. Amer. J.
Med. Sci., 175: 242, 1928.
K U G E L , M. A.: Congenital heart disease, cor biloculare. Amer. H e a r t
J., 8: 280, 1932.'
SHAPIRO, P . F . : Detorsion defects in
congenital cardiac anomalies. Arch.
P a t h . , 9: 54, 1930.
LIGHTNER, C. M . : An unusual case of
congenital malformation
of the
heart. J. Tech. Methods, 19: 148,
1939.
ABBOTT, M. E . : inOsLER, W.: Modern
Medicine. E d i t e d b y T . M c R a e ,
(8)
P E R N K O P F , E.,
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Tech.
AND W I R T I N G E R ,
W.:
Das Wesen der Transposition im
Gebiete des Herzens. Virch. Arch,
f. p a t h . Anat., 295: 143, 1935.
(9) SPITZER, A.: Uber den Bauplan des
normalen und miszbildeten Hertzens. Virch. Arch. f. p a t h . Anat.,
243: 81, 1923.
(10)
H A R R I S , J . S., AND F A R B E R , S.:
Trans-
position of t h e great cardiac vessels
with special reference to the phylogenetic theory of Spitzer. Arch.
P a t h . , 28: 427, 1939.