Paper - Cor biloculare, with a note on the development of the pulmonary veins (1937)

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Davies F. and Macconaill MA. Cor biloculare, with a note on the development of the pulmonary veins. (1937) J Anat. 71: 437-446. PMID 17104656

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This historic 1937 paper by Davies and MacConaill describes pulmonary vascular development.

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Cor biloculare, with a note on the development of the pulmonary veins

By F. Davies anp M. A. MacConaill

From the Department of Anatomy, University of Sheffield

  • This paper was read before the Anatomical Society at its Summer Meeting, June 1936.

The heart was taken from a boy 4 days old born in a state of blue asphyxia. The post-mortem examination showed no abnormalities of development other than those of the heart. We are indebted to Dr J. Clark, F.R.C.P. and Dr S. W. Wright, of the City General Hospital, Sheffield, for presenting the specimen to this department.1

External Appearance

(Figs. 1 and 2)

The heart presents a large right atrium: with appendix and a small left auricular appendix. The ventricular region shows no external evidence of division into right and left chambers. The infundibular region, however, is clearly marked and from it there proceeds a large arterial stem which gives off all the systemic arteries except the coronary arteries. In addition, a short distance from its commencement it gives off its posterior wall the right and left pulmonary arteries. A slender arterial channel, 2 mm. in diameter, passes downwards to the base of the ventricular region, behind the main arterial stem (Fig. 2). Here it ended blindly. Fluid injected downwards into it passed freely into the coronary arteries which arose near its lower end: but none passed into the ventricle. The floor of this channel is formed by three cushionlike projections from the wall of the vessel which correspond in position with the cusps of a normal aortic valve. The Y-shaped depression between the cushions is filled in below by a plate of tissue 1 mm. in thickness. The coronary arteries arose as normally from small sinuses of Valsalva. We identify the slender vessel as an ill-developed ascending aorta, cut off from the ventricle and serving merely as a feeder for the coronary circulation. The upper part of this aorta had been removed before we received the heart so that we were unable to determine its precise upper connexion.

Blake (1900) described a similar arrangement of diminutive ascending aorta with atresia of the aortic orifice. In his case the pulmonary arterial stem continued directly by means of a large ductus arteriosus into the descending aorta, while the diminutive ascending aorta arose from the lower aspect of the right end of a common brachio-cephalic trunk, which in its turn represented the transverse part of the arch of the aorta. Blake noted the reversal of blood flow in the ascending aorta, whose sole function, as in our case, was to feed the coronary arteries.

Fig. 1. Heart viewed from in front.

Fig. 2. Heart viewed from behind.

In our specimen we identify the arterial trunk continued from the infundibulum as the pulmonary stem as far as the origin of the right and left pulmonary arteries. Between the latter point and the origin of the systemic arteries the vessel probably represents an enlarged ductus arteriosus. Beyond the origin of the systemic arteries the vessel continued as descending aorta.

The terminal parts of the great veins have an unusual arrangement. The right superior vena cava is of small diameter; the coronary sinus is large and is continuous with a left superior vena cava. Between the sites of entrance of these veins is a sac, the wall of which is continuous with part of the dorsal wall of the atrium. The inferior vena cava enters this sac below and to the left, and an upper and a lower pulmonary vein enter it above and to the right. On opening the sac from behind it is found to be bounded in front by a vertical septum-like fold and to communicate with the right atrial cavity by a slit to the left side of the fold, and with the cavity of the left auricular appendix through a smaller opening. The nature of this sac and of the septum-like fold will be considered at a later stage.

The Interior of the Heart

(Fig. 3)

The heart shows an apparently single atrium and ventricle separated by a well-marked annular ridge, from which arose an atrio-ventricular valve of three cusps. The left auricular appendix is present so that the heart is essentially bi-atrial. A rudimentary septum inferius is also present, so that the heart is essentially, but very incompletely, biventricular. The heart is thus physiologically bilocular but morphologically quadrilocular.

Atrial region

The atrial chamber receives the openings of the right superior vena cava and coronary sinus and, between them, the slit-like opening of the sac which has been seen to take the terminations of the pulmonary and inferior caval veins. A large thick trabeculum lies between the opening of the sac and the right superior cava. The right boundary of the opening into the sac is formed by a projecting fold which passes upwards to bound the right and upper parts of the superior caval opening, and downwards to fuse with the upper part of the valve of the coronary sinus. We identified this fold as a persistent and enlarged — right sinus valve; and confirmed our identification by histological examination of its structure as described later. The sac is a smooth-walled cavity, divided into an anterior and a posterior part by a low, sharp ridge which extends across its floor from right to left, just in front of the termination of the inferior vena cava, and blends with the base of the right sinus valve. The opening of the left auricular appendix is anterior to it. The relations of the atrial sac to the right venous valve, and the presence of the ridge in its floor lead us to identify it as a persistent part of the sinus venosus (behind and above the ridge) and common auricular chamber (in front of the ridge), and we have, therefore, to record a persistence of separate sinus venosus with the pulmonary veins and inferior vena cava opening into it. There is no trace of either septum primum or septum secundum. The atrial cavity thus comprises three parts: (1) a middle or common auricle, which lies anterior to the ridge in the floor of the atrial sac and between the right sinus valve on the right side, and the opening of the left auricular appendix on the left; (2) the right atrial cavity and appendix; and (3) the left auricle, represented by the auricular appendix, which has the usual spongy structure.

Fig. 3. Interior of heart—dissected from in front.

Ventricular region

The walls of the ventricular chamber are heavily trabeculated. The wide, single atrio-ventricular orifice is guarded by a valve of three complete cusps, which resemble the tricuspid valve of the normal right ventricle in their topographical position. The cusp analogous to a septal cusp springs from that part of the atrio-ventricular limbus which lies below and to the left of the opening of the coronary sinus. It is large, and both it and the analogue of the normal anterior (infundibular) cusp receive chordae tendineae from a papillary muscle, which arises from a prominent fleshy ridge on the dorsal and inferior aspects of the ventricular wall. We shall adduce evidence later to show that the fleshy ridge is a rudimentary septum inferius. On the ventricular aspect of the subcoronary cusp, and between it and the septum inferius, there is a small space, open below and closed above. The slender ascending aorta comes down to a point just above the blind end of this space, which may thus be identified as the locus of the aortic vestibule. The large arterial stem (pulmonary stem) lies above and to the left of the septum inferius and the papillary muscle which springs from it. The junction between this artery and the ventricle is guarded by a fully developed semilunar valve of three cusps, each cusp being opposite a well-defined sinus of Valsalva. The cusps have the same topographical disposition as those of the normal pulmonary stem. The right and left pulmonary arteries open from the posterior wall of the pulmonary stem; the right artery arising at a lower level than the left. The right pulmonary vein enters the heart at a lower level than the left. The right lung bud descends to a lower level than the left in its early stages, and the pulmonary vessels collectively thus show some retention of their early ontogenetic relationships.

The Conducting System

Histological examination of blocks removed from various sites resulted in evidence which corroborated the previous conclusions which we had reached concerning the morphology of the appropriate regions. Typical sinu-atrial nodal tissue was observed in the fold on the right side of the right superior vena cava, and in the upper part of the fold on the right side of the entry of the sac which received the pulmonary veins and inferior vena cava. This was taken as indicating that the fold which continued down from the right side of the opening of the right superior vena cava, on the right of the sac and thence on the right of the opening of the coronary sinus, is the right sinus valve. No nodal tissue was found in the muscular band to the left of the opening of the sac.

The atrio-ventricular node was found to the left of the opening of the coronary sinus, at the junction of atrial and ventricular walls, and beneath the base of the “septal” (posterior) cusp of the atrio-ventricular valve. Distally the atrio-ventricular node continued into the atrio-ventricular bundle, which ran in the muscle ridge previously suspected to be the abortive septum inferius. Beneath the “septal papillary muscle” which projected from the ridge the atrio-ventricular bundle divided into right and left limbs, which coursed distally on either side of the septum inferius and at its lower part spread out beneath the endocardium. The right limb has its typical round form and the left its flattened appearance. These faets corroborate the opinion that the muscle ridge is the septum inferius, the atrio-ventricular bundle, as normally, at its bifurcation straddling the upper border of the septum.

The disposition of the conducting system makes it clear that the abnormalities of this heart are pure defects in development. Of the three distal septa (aortico-pulmonary, distal bulbar, and proximal bulbar) the aortico-pulmonary and distal bulbar septa have developed normally; so that the aorta and pulmonary artery have been normally formed from the common primitive trunk. The proximal bulbar septum, however, has failed to form. The anlagen of the aortic semilunar cusps, although formed in their correct positions, have fused together, thus cutting off the aorta from the bulbo-ventricular cavity. The ventricular septum (septum inferius) has lagged behind in development. The auriculo-ventricular canal has remained undivided. The presence of three cusps has, we think, no special significance; for cases of bilocular heart may show from two to five cusps in the atrio-ventricular valve (Wood & Williams, 1928).

The Development of the Pulmonary Veins

The atrial abnormalities of this heart are explained by reference to the early developmental stages of the pulmonary vein. This vein is generally described to be present as a single vessel—common pulmonary vein—in human embryos of 5 mm. greatest length, and in other mammalian embryos at corresponding stages of intra-uterine development. The earlier stages are less well known. Flint (1906) concluded that the vein (pig) is an outgrowth from the sinus venosus, which establishes communication with the vascular plexuses of the embryonic lungs. Brown (1918) holds that the pulmonary vein (cat) is merely a specialized part of the pre-splanchnic venous plexus which opens into the dorsal part of the sinus venosus. Buell’s results (1922) combine those of Flint and Brown. On the one hand, he describes the common pulmonary vein (chick) to be formed from angioblastic cells which grow out from the dorsal wall of the sinus venosus. On the other hand, he describes the four pulmonary veins of the adult form to arise as part of an angioblastic splanchnic plexus. The angioblasts of both the common pulmonary and the four definitive pulmonary veins undergo a central liquefaction, and fuse to form a common pulmonary vein with four ultimate tributaries. The position of the opening of the vein on the dorsal wall of the sinus is primarily central (Flint, 1906; Brown, 1913; Fedorow, 1908, 1910; Bremer, 1928); although Tandler (1912) first describes it to be in the left atrium, and Spitzer (1923) makes it enter a chamber (pulmonary sinus) distal to the sinus venosus and to its left side—essentially the left atrium. It seems to us that one factor in the division of the sinu-atrial region into right and left chambers has not received due recognition: namely, the active part played by the common pulmonary vein itself in the process. It is with this factor that the present observations are particularly concerned.

A human embryo of 4-5-5:0 mm. greatest length shows the common pulmonary vein as a wide channel entering the heart at the dorsal wall of the auricular region in the median plane. This entrance was 60 above, and to the left side of, the most cranial part of the right sinus valve. There is no left sinus valve in this embryo: that is, the dorsal wall of the middle part of the sinus venosus is completely continuous with the dorsal wall of the middle part of the auricular region. An auricular septum (septum primum) is present in the dorsal and cranial parts of the auricular wall. Its caudal extremity is at the cranial part of the right of the pulmonary vein. The right wall of the pulmonary vein is definitely invaginated into the cavity of the common auricle, forming a pulmonary fold. This fold is not the septum primum, but is a distinct formation to the left side. of it. The cranial extremity of the pulmonary fold is fused with the left side of the septum primum which extends caudally along the left side of the upper third of the pulmonary fold. We believe that this pulmonary fold is homologous with the pulmonary fold described by Robertson (1914) in the embryonic heart of Lepidosiren, and that it plays a similar part in the separation of the auricular chambers. The right wall of the pulmonary vein of Lepidosiren elongates, invaginates the sinus, and makes its way across the cardiac cavity to the anterior endocardial cushion. Cranial to it is the septum primum, caudal to it is the cranial surface of the cushion. It fuses with both, thus playing an active part in such separation of the , right and left atria as is effected in this animal. Since the right wall is elongated it follows that the opening of the vein becomes directed to the left, that is, the vein determines its own opening into the left atrium. In short, the atrial septum of Lepidosiren consists of three elements: the septum primum, the pulmonary fold, and the anterior endocardial cushion; and of these three, the pulmonary fold alone is operative in directing the pulmonary blood to the left side of the heart. Chun Chang (1931) has similarly described an endothelial fold at the right side of the pulmonary vein (in the chick) Fig. 4. Interior of auricular region of heart of as an essential constituent of the human embryo, 4-5-5-0 mm. greatest length, inter-atrial septum. Buell (1922) has viewed from below, based on contour recondescribed in the chick embryo an elongation (and thickening) of the right wall of the common pulmonary vein (stage of 50 hours’ incubation). Both Brown and Buell identified this fold with the left valve of the sinus venosus: whereas Fedorow thought it a part of the auricular floor. In view of the fact that the left sinus valve fuses with the right side of the atrial septum, and that the pulmonary fold, as we describe it, is on the left side of the septum primum and fuses with it on that side, we hold that the left sinus valve is a distinct structure from the pulmonary fold. It seems in fact to differ in its degree of development in different groups of vertebrates; and it is definitely absent (Robertson, 1914) in Lepidosiren, in which the pulmonary fold makes its first appearance. The part the pulmonary fold takes in determining the ultimate topography of the atrial region is made clear by reference to a still earlier stage of human development.

In a human embryo of 2-2 mm. greatest length we observed a channel, lined by endothelioid cells, running obliquely caudally in the dorsal mesocardium, from the ventral pharyngeal wall to the dorsal wall of the sinus venosus. It invaginates the sinus venosus in the median plane, just proximal to the sites of entrance of the omphalo-mesenteric veins. We did not find it opening into the sinus; but, to reach the wall of the sinus, it turned quite sharply forwards, as was confirmed by a wax-plate reconstruction of the region (at 150 diameters); and its lower part contained a few nucleated blood corpuscles. The definitely tubular nature of this channel, the direction of its course, and the presence of blood cells, differentiate it from the simple mesocardial cysts described by Davis (1927). In its position it corresponds to the anlage of the common pulmonary vein as described by Robertson in Lepidosiren, and by Buell in the chick (8 hours’ incubation); and by Brown in the cat, and by Flint in the pig, under the name of “ cranial splanchnic tap”. Accordingly we identify this endothelioid channel as the primitive common pulmonary vein; and record that it is related at its termination to the dorsal wall of the sinus venosus in the median plane, cranial to the level at which the omphalomesenteric veins enter the heart. It is, then, morphologically a median (cranial) splanchnic vein, as Brown maintained; and it shares this relationship with the vitello-umbilical veins, which are, collectively, its caudal counterpart. The three veins are primarily related to the middle part (or body) of the sinus venosus; and this relation is emphasized as the right and left horns of the sinus enlarge. The transference of the opening of the pulmonary vein to the left atrium is then the work of the pulmonary fold. Should this not form and a partial atrial septum (septum primum) be present, then the vein (or its tributaries) may appear as opening wholly or partly into the right atrium; as has been described by Rokitansky (1875) and others: these cases are, of course, to be distinguished from such a case as that cited by Spitzer (1923) in which an abnormal septal formation took place within the left atrium to the left of the opening of the pulmonary veins. In the present case both septum primum and pulmonary fold have failed to develop; the common pulmonary vein has been absorbed into the wall of the middle part of the sinus, and is represented by that part of the wall of the sac immediately posterior to the middle part of the right sinus valve; this part of the cavity of the sac may properly be called the pulmonary sinus. The right and left horns of the sinus have been cut off from the middle part by sinus septa (limbic bands) and are represented by the openings of the superior vena cava and coronary sinus respectively; and the inferior vena cava (omphalo-mesenteric element) has retained its primitive morphological position as the caudal of the two splanchnic taps which open into the middle part of the sinus venosus on its dorsal wall. Cor Biloculare 445


This case appears to be unique. No parallel instance appears in the cases described by Rokitansky (1875), Symington (1900), Paterson (1909), Keith (1909), Walmsley (1929). Spitzer (1923), Abbott (1931), or Bredt (1935). Ratner e¢ al. (1921) describe a case of dextrocardia in which the ventricles are fully separated, but the atrial septum is completely absent. In this case, although there is a transposition of the ventricles, yet the superior and inferior caval veins open into the right side of the atrial chamber, and the four pulmonary veins open to the left of the caval veins. The two right pulmonary veins enter the heart to the right side of the median plane, and the other two open to the left of it. The superior vena cava opens into a dilated chamber which in turn enters the atrium, and which Huntington identified as a persistent part of the right omphalo-mesenteric vein. It is, then, a sac of quite a different nature from that which we have described; and the same remark applies to the sac described by Zimmermann (1934)—a simple diverticulum of the atrium. The several deficiencies in development in our case combine to give a picture of an extremely primitive heart. This heart, however, has its own specializations. Walmsley (1931) has already stressed the potential independence of the bulbo-ventricular from the other parts of the cardiac tube with respect to its development. The expulsive parts of the heart we have described illustrate this independence in the case of their formations. We wish to draw attention to a similar independence of the process of incorporation of the stem of the pulmonary vein into the wall of the sinus venosus, and the process of formation of that essential element of the complete atrial septum to which we have applied the name “‘ pulmonary fold’. In our case the latter process has failed to take place, but the former has occurred. Such an independence is understandable upon the postulate that quite different mechanisms are responsible for the two phenomena: namely, that the formation of the pulmonary fold is a property of the developing tissue as such (and may be suppressed); while, the widening of the ostium venosum pulmonale, which results in the incorporation of the venous stem in the wall of the atrium, is perhaps a purely physical response to the back pressure of the blood. Bremer (1928) has already indicated how dependent is the normal course of development of the heart upon a balance of the morphological and physical properties of the cardiac tube.


  1. A case of congenital abnormality of the heart is described in which there is complete absence of atrial septa and of the proximal bulbar septum. The septum inferius is rudimentary. There is atresia of the aortic orifice and only the coronary arteries arise from the diminutive ascending aorta.
  2. A small right, and a large left, superior vena cava open into the right part of the atrium. The sinus venosus has been incompletely absorbed and the inferior vena cava and the two pulmonary veins open into it.
  3. Histological study of the conducting system verifies the conclusions arrived at concerning the morphology of the different parts of the heart.
  4. The early stages in the development of the common pulmonary vein in man are examined and attention is drawn to the active part played by the pulmonary fold in the separation of the right and left parts of the primitive atrium.

We wish to express our thanks to our technical assistant Mr J. T. A. Hall for help with the section-cutting and photography which this work has entailed.

A.A, Ascending aorta.

ALD. Entry to aortic vestibule. A.V.C. — Atrio-ventricular canal.

BC Bulbus cordis

CS. Coronary sinus.

I. Infundibulum.

I.V.C. Inferior vena cava.

L.A. Left atrium.

L.Ap. Left auricular appendix.

L.P.A. Left pulmonary artery.

L.P.V. Left pulmonary vein.

L.S.V.C. Left superior vena cava.

O.L.A Opening of left auricle into sac. O.R.A Opening of right auricle into sac. P.A Pulmdnary artery (stem).


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Brown, A. J. (1913). Anat. Rec. vol. vit.

Bust, C. E. (1922). Contr. Embryol. Carneg. Instn, vol. x1v.

Cuun Cuane (1931). Anat. Rec. vol. L.

Davis, C. L. (1927). Contr. Embryol. Carneg. Instn, vol. x1x. Frporow, V. (1908). Anat. Anz. vol. xxxmr.

—— (1910). Anat. Hefte, Abt. 1, Bd. xx.

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Kerra, A. (1909). Lancet, vol. 11.

Paterson, A. M. (1909). J. Anat., Lond., vol. x11. Ratner, B., Apport, M. E. & Beatriz, W. W. (1921). Amer. J. Dis. Child. vol. xx11. Roserrson, J. I. (1914). Quart. J. Micr. Sci. vol. t1x.

v. Roxrransky, C. (1875). Die Defekte der Schiedewand des Herzens. Vienna.

Spitzer, A. (1923). Virchows. Arch. vol. ccXLIM. Symineton, J. (1900). J. Anat., Lond., vol. xxxtv. TANDLER, J. (1912). In Kresen & Matt, Human Embryology, vol. 1. Watms.ey, T. (1929). Quain’s Anatomy, vol. tv, pt. 3, passim.

—— (1931). J. Anat., Lond., vol. txv.

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P.F. P.V. R. R.A. R.P.A. R.P.V. RSV. RSV.C.

Pulmonary fold.

Pulmonary vein.

Ridge in floor of sinus venosus.

Right atrium.

Right pulmonary artery.

Right pulmonary vein.

Right sinus valve.

Right superior vena cava.

Entry of sac (which receives inferior vena cava and pulmonary veins).

Systemic branch (of arterial stem).

Septum inferius.

Septum primum.

Septal papillary muscle.

Sinus venosus.

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