Paper - On the development of the atrial septum and the valvular apparatus in the right atrium of the pig embryo (1916)

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Morrill CV. On the development of the atrial septum and the valvular apparatus in the right atrium of the pig embryo, with a note on the fenestration of the anterior cardinal veins. (1916) Amer. J Anat. 20(3): 351-374.

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On the Development of the Atrial Septum and the Valvular Apparatus in the Right Atrium of yhe Pig Embryo, with a Note on the Fenestration of the Anterior Cardinal Veins

C. V. Morrill

Department of Anatomy, Cornell University Medical College, New York City

Nine Figures


The method of formation of the atrial septum and nearly related parts in the mammalian heart has been known since the careful investigations of Rose ('88 and '89), Born ('89), and more recently Favaro ('13). These writers are in substantial agreement regarding the structures concerned in this process, though differing in some respect as to detail. The now classical work of Born on the rabbit has been used extensively as a basis for descriptions of cardiac development in some of the more recent text-books of embryology, notably by Hochstetter ('01-'03) and Tandler ('12 and '13). Born in his account, which included some observations on human embryos, corrected the error of His ('85) regarding the formation of the atrial septum and its relation to the foramen ovale. His description differed from the earher one of Rose ('88) in several important respects but later Rose ('89) accepted Born's corrections. Rose and Favaro extended their observations to a number of different mammals, but not, as far as I am aware, to the pig. Retzer ('08) published a brief note on the development of the heart in which he claimed that Born's account of the atrial septum in the rabbit could not be applied to the pig. Since pig embryos are extensively used for study in American laboratories, it seemed advisable to re-examine the development of the septal and valvular apparatus in this form in order to clear up any uncertainty which may exist regarding the processes involved.'

This study is based on series of pig embryos of 6.8, 7.9, 8.5, 12.3, 15.2 and 21 mm. total lengths, supplemented by dissections of the hearts of foetuses from the 45 mm. stage to birth. The hearts of the 7.9, 15.2 and 21 mm. embryos were reconstructed by the wax-plate method. In addition several human embryos from 7.6 to 22 mm. were examined for comparison.

The terminology of Born which has been largely adopted by other writers will be used, with some modifications, in this account.

In the stage represented by a 6.8 nmi. embryo, septum I forms an incomplete interatrial curtain. Ostium I is still widely open and ostium II has begun to form. In the reconstruction of a 7.9 mm. embryo (fig. 5), the relation of these three structures is shown. Septum I (S.I) though fused for the 'most part with the atrial walls, still presents a short, free border facing the now very narrow^ ostium I (O.I). In the posterior superior corner of the septum, the new opening or ostium II (O.II) is well advanced and much larger at this time than ostium I. It is apparent from the figure that ostium II is formed by fenestration in the pig and is not at first a single opening as Born found in the rabbit. Born thought that a primitively single opening was normal for mammals generally, but Rose found a fenestrated septum in three cow embryos, a mole embryo and two rabbit embryos and states that Bruch's observations on sheep, cow and horse and Rokitansky's- on a human embryo support the conclusion that fenestration is the more usual condition. Favaro found numerous orifices, representing ostium II in the sheep, but only a single opening in the guinea-pig. As a rule, Rose believes, the larger openings coalesce to form a single ostium II while the smaller ones close up.

1 This investigation was begun in the anatomical department of the University and Bellevue Hospital Medical College and completed at Cornell Univer.sity Medical College, New York.

The observations of Bruch and Rokitansky are known to me only through the brief mention made by Rose ('88).

Exceptionally the hitter may persist until birtli. In the pig later stages always show a single opening.

The closure of ostium I in the pig is effected in the same manner as described for the rabbit, guinea-pig, man and other mammals. This process is illustrated in figures 1, 2, 3, and 5. Septum I is composed for the most part of developing muscle which is continuous with the musculature of the roof, posterior wall and floor of the atrium. Its free border, however, is capped by a prominent endocardial thickening. As the septum grows downward and forward toward the atrial canal, the endocardial thickening develops two extensions or horns which fuse with the endocardial cushions of the atrial canal. The upper one blends with the upper cushion (fig. 1), the lower one with the lower cushion (fig. 3). Ostium I (fig. 2) is thus entirely surrounded by thickened endocardium except where it is continuous with the narrow slit (transverse fissure) between the endocardial cushions of the atrial canal. At a slightly later stage (8.5 mm.) the blending of the separate portions of endocardium is complete and ostium I together with the transverse fissure is closed. In the 15.2 mm. stage (fig. 6) ostium II iO.II) is much enlarged and forms a single large opening between the atria. Septum I {S.I) presents a very irregular free border which faces upward and sHghtly posteriorly toward ostium II. (The irregularity of the free border could not be represented in wax.) The septum as a whole bends toward the cavity of the left atrium.

The mode of formation of septum II (the later limbus Vieussenii) is first clearly indicated in the 7.9 mm. embryo though a faint trace is sometimes distinguishable in an earlier stage. Concerning the origin of this septum there has been some difference of opinion. Indeed Retzer ('08) has denied its existence in the pig, though Rose ('88 and '89), Born ('89) and Favaro ('13) have found it in all the forms they studied. Rose expressly stating that it is characteristic of all placental mammals. In the present study it will be shown that septum II is as definite and well developed in the pig as in any form so far examined.

The model of the 7.9 mm. embryo (fig. 5) shows a very distinct spur-like thickening {S.I I) which projects into the cavity of the right atiiuni in the angle between the fiooi- and septum I, and just x^osterior to ostium I (0.7). It is continuous with the left sinus valve. Trans^^erse sections through this region (figs. 1, 2 and 3) show that at first this spiir (S.II) is composed of connective tissue alone and is sharplj^ marked off, histologically, from the developing musculature of the sinus valves, septum I and the atrial floor. It appears to be nothing more than a projection, toward the right, of the endocardial thickening of septum I (S.I) and is continuous through the latter with the endocardial cushions of the atrial canal (En.s. and En.i.). This structure which is the anlage of septum II, is undoubtedly what His ('85) called the spina vestibuli and, taken together with the endocardial cushions, would constitute his septum intermedium. The lower end of the left sinus valve blends wdth it, while the corresponding end of the right valve flattens down in the atrial floor close to it (figs. 2 and 5, Vv.v.). At this stage, the anlage of septum II is not in relation with ostium II.

Figs. 1 to 3 Transverse sections of the h^art region of a 7.9 mm. embryo (histological structure semi-diagrammatic). Figures 1 and 3, above and below the level of ostium I respectively; figure 2, through ostium I. A., dorsal aorta; A.d., right atrium; ^.s., left atrium; En.s., upper endocardial cushion; En.i., lower endocardial cushion; O.I, ostium I;, interventricular septum; S.I., septum I; S.II, septum II; Sn.d., right sinus horn;, spatium interseptovalvulare;, and, right and left common cardinal veins; V.r.d., right sinus valve; Vv.v., sinus valves. Magnified about 2.5 diameters.

In later stages, when ostium I has completely closed, the spur lengthens out into a definite ridge. This is well shown in the model of a 15.2 mm. embryo (fig. 6, S.II). When traced from its point of origin in the anterior inferior corner of the atrium, this ridge extends upwards then bends backward along the roof toward the posterior wall where it flattens down and may become continuous with two or three muscular trabeculae w^hich develop in this region, i.e., the spatium intersepto-valvulare. These trabeculae are not constant in number. The portion of the ridge in relation to the roof of the atrium^ is broad and low contrasted with its low^er anterior end or root which is sharp and well-defined. Both sinus valves {V.v.s. and V.v.d.) now blend with it, the right, however, slightly covering its lateral side.

The internal structure of septum II is shown in a transverse section taken at about the middle of its anterior vertical portion (fig. 4, S.II). The endocardial thickenings which entered into its formation in an earlier stage, have fused together into a solid quadrilateral mass. A cap of developing muscle covers its posterior border (upper in the figure) and extends anteriorly for some distance along its lateral surfaces. This muscular mass is continuous with the musculature of septum I and, at a lower level (not shown in the figure), with that of the two sinus valves which, as mentioned, blend with the root of the septum. A careful study of serial transverse sections shows that the musculature of this part of septum II is derived from that of two simis valves and scptinu I. Tlie (levelopiiig inuycle elements appear to invade the connecti^'e tissue and gradually to replace it.-* This invasion has not yet begun in the 8.5 mm. embryo but is well advanced in the 12.3 mm. and s'ill more so in the 15.2 nmi. described above. The anterior portion of the connective tissue mass or septum intermedium^ (fig. 4 En.c.) broadens out in a lateral direction between the two atrio-ventricular orifices and is joined by the interventricular septum, the line of fusion being toward the right. ^ The fusion is not complete, however^ for the interventricular ostium (fig. 6, is still widely open at this stage. If septum II is now traced upward and backward into the roof of the atrium, the connective tissue elements gradually disappear and it appears as a low, broad thickening of the atrial musculature which follows the external depression caused by the bulbus in this region. It is not, however, due to an infolding of the atrial w^all, but to a local increase in the developing muscle elements. This upper part of septum II now comes into relation with ostium II (fig. 6, O.II) which meanwhile has become much larger.

^ Owing to the position of the model this part of septum II is hidden in figure 6.

Fig. 4 Transverse section of the heart region of a l.l.L' mm. embryo at the level of the root of septum II (histological structure semi-diagrammatic). A., dorsal aorta; A.d., right atrium; A.s., left atrium; En.c, fused endocardial cushions;, interventricular septum;, spatium intersepto-valvulare; S.I., septum I; S.IT, septum II; and right and left common cardinal veins. Magnified 25 diameters.

Passing now to the 21 mm. embryo, the further development of septum II (fig. 7, *S.77) is clearly shown. It appears as a crescentic ridge extending from the lower inferior corner of the atrium, upward and backward toward the posterior wall. Its lower segment or root which is thickest and most sharply defined is partly hidden by the high right sinus valve iV.v.d.) which blends with its lateral surface. Traced upward it curves over the roof of the atrium bordering ostium II {O.II) and reaching the posterior wall, bends downward somewhat in the region of the spatium intersepto-valvulare (not shown in the

^ The invasion of the connective tissue mass (septum intermedium) by the musculature of the sinus venosus was described by Retzer ('08) as the source of the Purkinje fibres in the ventricles. The present investigation leads to the conclusion that a part of this muscle, at least, thickens to form the root of septum II.

'" The term 'septum intermedium' originally used by His ('85), may be conveniently retained for this structure as suggested by Favaro ('13), although Born and some others discarded it.

" A portion of the septum intermedium thus separates the right atrium from the left ventricle (conus arteriosus of the aorta) forming the septum atrioventriculare of Hochstetter. figure). This upper segment is broad and low where it faces ostium II but becomes narrow and sharp in the posterior wall. Septum I meanwhile has changed its position relative to septum II, so that its free border now faces upward and forward, and ostium II has become an oblique cleft, the definitive foramen ovale, between the septa.

Before considering the later changes in septum II it will be convenient to compare the conditions found in the pig with those described for other forms. According to Born septum II first appears (rabbit and man) in the upper part of the posterior wall of right atrium a little to the right of septum I. It is a crescentic spur which encroaches upon the spatium interseptale and forms the principal part of the limbus Vieussenii. In the pig irregular muscular ridges develop in the same locality but they vary greatly in form, size and number. In the model of the 15.2 mm. embryo, two such ridges can be distinguished (fig. 6). W^ien septum II has extended backward to the posterior wall, one or more of these ridges is incorporated in it, but no one of them is sufficiently well-marked to be taken as a starting point for the developing septum. Further, at the time when the anlage of septum II is first distinguishable in the lower anterior wall (7.9 mm. embryo) the spatium intersepto-valvulare is relatively very wide and numerous small irregular ridges api^ear in its upper posterior wall. Along with the narrowing of the spatium, the ridges decrease in number until finally they are reduced to one or two which, as stated, are incorporated in the septum.

An examination of several human embryos seemed to indicate that much the same sort of process takes place there. In an embryo of about 12 mm., total length, at least three muscular ridges could be distinguished in the upper, posterior wall of the spatium intersepto-valvulare, while in one of about 14 mm. only one such ridge appeared which, however, was quite prominent." In the lower anterior part of the right atrium of both these embn'os there was a thick coiiiu'ctive tissue ridge or prominence continuous with tlie fused endocardial cushions and partly overlaid and invaded by developing muscle. As in the pig this musculature was continuous with that of septum I and the sinus valves. The resemblance between this structure and that described for the pig in the corresponding place is so close that I am inclined to think it represents the origin of septum II in man. Indeed Thyng ('14) in his description of a human embryo notes the presence of a ridge or tubercle" in the same region and states that "from the relation which the tubercle bears to the septum primum and the left sinus valve it can scarcely be doubted that it would eventually form part of the adult limbus fossae ovalis."

Through the kindness of Dr. Thyng I have hiid the opportunity of examining the human embryo which formed the subject of his paper ('14). In this specimen (17.8 mm.), the region of the spatium intersepto-valvulare was entirely devoid of muscular ridges.

Born seems to have overlooked the early appearnace of this ridge entirely, though he states that in man the bay of the crescent (septum II) swings further downward in later stages and finally unites with the lower end of the left sinus valve. He thus includes the region in which the ridge is found in the pig. In the rabbit, however, septum II remains as a narrow short crescent in the anterior upper wall of the atrium. One may conclude from this that the ridge if present at all is poorly developed in this animal.

Rose ('89) in summarizing the results of his earlier work ('88) speaks of septum II (limbus or annulus ovalis) as follows:

On the anterior and upper atrial wall there appears a ridge-like infolding, the septum musculare which, together with the septum intermedium is formed into a closed ring diaphragm, the

annulus ovalis The septum intermedium arises from a

connective tissue spina vestibuli overlaid, however, on its upper surface by a thin continuous muscle layer, which unites with the broad atrio\entricular cushions, the latter fused together in the middle.

It is apparent that this description corresponds very closely with that given for septum II in the pig with the exception that the upper part of this septum corresponding to Rose's septum musculare is not formed by an infolding of the atrial wall but by a local thickening. In his later paper ('89) following Born's work. Rose modified his description of the atrial septa extensively. He rejected the idea that the septum intermedium is concerned in the formation of the Hmbus or annulus ovaUs. He also discarded the term 'septum musculare,' calling it simply the limbus (Vieussenii) and described it as arising in the anterior upper atrial wall as an infolding caused by the truncus arteriosus (bulbus) imbedding itself between the two atria. From here it spreads along the upper and then along the lower wall of the right atrium. It contains a connective tissue core which was pinched off from the surface of the truncus during the process of infolding. The presence of this core, Rose thinks, is a proof that infolding has occui*red.

In the pig the upper part of septum II or limbus which corresponds to the curve of the bulbus, is at first a broad thickening of the musculature of the atrial wall which in later stages becomes more prominent. Only in its lower anterior part or root are connective tissue elements found. These are the remains of the original thickened endocardium which was show^n to form the basis for the septum. Retzer ('08) in denying the presence of a septum II in the pig says: "This supposed septum which His correctly described as a 'muskulose Leiste' is nothing but a fold in the atrial wall at that place." It is formed by the atrial growing around the conus arteriosus as a fixed point, thus causing a bulging inwards of the atrial wall.

The descriptions of Rose and Retzer thus correspond quite closely as far as the origin of the muscular fold is concerned. Retzer, however, thinks it never attains sufficient size to be called a septum. His ('85) described the same structure, calling it the anterior septum or 'sickle' which later gives rise to the limbus Vieussenii. He thought that it was formed by the septum intermedium growing up on the anterior atrial wall to meet the anterior end of the septum superius (septum I). This upgrowth of the septum intermedium, or a portion of it overlaid by muscle, is practically what takes place in the pig, but as pointed out previously, there is no evidence of an infolding of the atrial wall at a higher level.

Favaro's ('13) recent account of the septum secundum in the guinea-pig and sheep differs very little from that given above for the pig. He finds that the niyocardiuiu whicli invades the connective tissue of the septum intermedium becomes more compact and raised up into a distinct prominence on the right side of the insertion of the atrial septum (septum I). This, he says, represents the site of the inferior segment of the Hmbus fossae ovaUs. The prominence is continued upward as a thickening of the myocardium of the ventral wall of the atrium on the right of septum I. It corresponds to a broad sulcus externally but there is no infolding as described by Rose and Retzer. In the guinea-pig and sheep, however, Favaro finds that the septum spurium or tensor valvulae bends over the upper wall to join the newly-found Umbus or septum II. This does not occur in the pig as reference to figures 5, 6 and 7 will show. In this form the tensor valvulae^ {T.vv.) extends upward to the roof of the atrium where it is lost sight of among the developing trabeculae in that region. In the human embryos examined the course and relations of the tensor seemed to be more like those in the guinea-pig and sheep as described by Favaro.

From the first the lower end of the left sinus valve blends with septum II as mentioned previously. The right valve is at fii'st independent of the septum (fig. 5) but later when the septum has increased in height, the valve becomes attached to its right side (figs. 6 and 7). In later stages the right valve increases rapidly in height so that when seen from the right side, it completely covers the lower end of the left valve and the root of septum II (fig. 7). When a portion of the right valve is cut away (fig. 8) the connection between the left valve and septum II can be seen. Separating the orifices of the inferior vena cava {V.c.i) and the coronary sinus^ {Snxor.) is a thick ridge, the sinus septum (, which extends from the root of septum II downward and to the right toward the attached border of the right sinus valve, where it blends with the floor of atrium. Owing to the extreme height of the right valve the inferior vena cava and coronary sinus appear to open into a common chamber flanked by the valve.

^ The term 'tensor valvulae,' first proposed by Rose ('89), seems more appropriate than the older 'septum spurium' of His. This structure probably helps to approximate the valves and render them tense during systole.

' When the model was sawn through, the cut opened the right extremity of the coronary sinus which forms a deep bay as it turns backward and upward to its orifice (figs. 7 and 8).

The further changes in the right atrium may now be considered. From the 21 mm. stage (figs. 7 and 8) up to about 58 mm. the relations of the parts in question change very little. Septum I or the valvula foraminis ovalis, as it may now be called, becomes thinner and somewhat folded. Its free border is fimbriated. The left sinus valve is still well developed, its lower end blending with the root of septum 11. It now lies so close to the septal wall of the atrium that the spatium intersepto-valvulare is reduced to a narrow cleft. The right sinus valve remains high, guarding the orifices of the inferior cava and coronary sinus. The sinus septum between the two orifices is behind and medial to the valve but not fused with it. In two specimens (58 to 62 mm.) and possibly a third, a new opening appeared in the lower anterior part of the right sinus valve close to its attached border. The course of the blood-stream from the coronary sinus in this case was directly into the lower anterior part of the atrial cavity rather than upward, backward and medially toward the foramen ovale. The usual pathway, however, was not shut off. His ('85) described a secondaryopening of the coronary sinus in human embryos and assumed that it represented the normal condition. Other writers have not found this new opening, Born expressly denying its existence. It probably occurs exceptionally in man as in the pig and may represent a premature degeneration of this part of the valve.

The tensor valvulae (septum spurium) in the older foetuses becomes flattened down considerably in its upper part, though still fairly well marked near the sinus valves. Meanwhile a new muscular ridge, the crista terminal] s has appeared in the atrial wall just to the right of the right valve. Its upper part blends with the trabeculae in the roof of the atrium near the tensor valvulae. Traced downward it passes first close to the attached border of the valve and then diverges from it more and more until it is lost uniong the trabeculae of tlie lateral wall of the atrium. The right sinus valve does not seem to take any part in its formation, though both Rose and Tandler ('13) consider that the upper part of this valve is involved.

The final disposition of the various parts of the septal and valvular apparatus is shown in figure 9 which represents a dissection of the heart of a foetus of about 85 mm. Owing to the preponderating growth of the upper part of the atria, the region of the septa appears sunken into the entrance of the inferior cava, while the orifice of the superior cava (V.c.s.) remains high up on the posterior wall. Septum I, now the valvula foraminis ovalis (V.f.o.) lies in the bottom of a slight depression or fossa whose margin is formed for the most part by the limbus fossae ovaHs (L.V.). The free, fimbriated border of the valvula extends obliquely into the cavity of the left atrium and overlaps the limbus on that side. The oblique cleft between them is the foramen ovale. Above the fossa and extending downward on each side of it, the Umbus is thick and muscular. This part is formed by septum II.

Continuous with the anterior end of septum II is the left sinus valve {V.v.s.) which in this place is muscular like the septum and may be said to form part of the limbus. When traced backward and upward around the fossa, the valve becomes reduced to a thin, pale streak which finally crosses the posterior part of the Hmbus proper and then extends along the left margin of superior caval orifice where it gradually fades out. This is practically in agreement with the descriptions given by Born, Rose and others.

The right sinus valve {V.v.d.) is still well marked at this stage. Its lower anterior part bounds the orifice of the inferior cava laterally and extending forward and medially partially covers the orifice of the coronary sinus. The first portion represents the vah^la Eustachii, the last {X in fig. 9) the valvula Thebesii of other mammals. In the pig the right sinus valve never becomes divided structurally. There is always a narrow cleft between it and the sinus septum { The upper part of the right valve extends as a thin narrow membrane along the right border of the superior caval orifice ahnost to its upper end. The tensor valvulae has entirely disappeared.

At this stage the crista terminalis (Cr.ter.) forms a thick ridge extending downward from the roof, in the angle between the posterior and lateral walls of the atrium. It was pointed out that when the crista first appears it is entirely independent of the right sinus valve, but as it becomes broader and more fully developed, the extreme upper part of the valve comes to lie right on its root. There is usually, however, a narrow cleft separating it from the remains of the valve below. For this reason, the crista terminalis of the pig cannot be said to mark exactly the boundary between the primitive sinus cavity and the atrium proper as has been maintained by His, Rose and Tandler for man.

A glance at figure 9 will show that there is a broad, rounded ridge in the angle between the orifices of the superior and inferior venae cavae (the line marked V.v.s. passes across it). It is formed by a thickening of the musculature of the atrial wall in this region and represents the tuberculum intervenosum (Loweri) of the human heart. There has been some doubt about the occurrence of this structure but recently Tandler ('13) came to the conclusion that it is always present in the adult human heart if hardened in situ, i.e., with the pericardium intact. He suggests the term 'torus Toweri' as more appropriate. In other mammals he finds it more strongly developed than in man, especially in the horse and still more so in the seal where it forms a 'veritable septum.' In the pig this ridge occurs constantly in older foetal stages. Owing to its position it would tend to direct the blood-stream from the superior cava toward the right atrio-ventricular orifice.

The chief results of this investigation may be summarized briefly as follows :

In the pig, the method of formation of septum I and ostia I and II is essentially the same as described in other mammals.

The present account of septum II, however, differs considerably from those of other writers with the exception of Favaro. The anlage of this septum in the pig appears in the lower anterior c'onu'f of tlie right atriiiiii. It is a spur-like thickening developed on the right side of the line of insertion of septum I and is composed, at first, of connective tissue. Later it lengthens out and becomes overlaid and invaded by developing muscle. It then extends upward and backward along the roof of the atrium as a low, broad thickening of the musculature in this region and finally reaches the posterior wall where it bends downward as a narrow, sharp ridge. For the reasons stated in the text, I am inclined to believe that septum II is formed in the same manner in the human embryo.

The right sinus valve is well-developed in the pig. Its lower part guards the orifices of the inferior vena cava and coronary sinus in later stages but does not become divided by the sinus septum into Eustachian and Thebesian valves as in other forms.

The crista terminalis develops independently of the tensor valvulae (septum spurium) and right sinus valve. It does not accurately mark off the primitive sinus cavity from the atrium proper.

A tuberculum or torus Loweri is always present in older foetal stages.

One further point which is illustrated by the models may be mentioned although it is not directly related to the subject of this paper, namely, the fenestration of the proximal part of the anterior cardinal vein. In the 7.9 mm. embryo (fig. 5, this process is well advanced and many of the fenestrae have coalesced, thus tending to separate off a dorsal portion of the cardinal which would receive the intersegmental veins in this region. In the 15.2 mm. embryo (fig. 6, the separation is complete up to the point where the subclavian vein (V.scl.) enters. On the left side (not shown in the figure) where the subclavian appears to enter one segment higher (cephalad) than on the right, the separation is carried upward correspondingly. These observations support the opinion of Thyng ('14) that the proximal part of the vertebral vein is segregated from the main venous channel (anterior cardinal) in the manner described. In an earher paper Thyng ('11) figured this condition in a pig embryo of 7,8 mm. Lewis ('03) mentions a splitting of the anterior cardinal vein near its entrance into the duct of Cuvier, the subclavian vein arising from its outer part. A comparison of his Plate IV and Thyng's ('11) figure 2, with figures 5 and 6 of the present paper seems to indicate that this process is normal for the pig embryo.

In conclusion I wish to express my thanks to Prof. H. D. Senior who kindly suggested a re-investigation of the atrial septum and to Prof. F. W. Thyng for advice and criticism.


BoRX, O. 1888 ttber die Bildung der Klappen, Ostieu und Scheidewiinde in

Siiugerthicrherzens. Anat. Anz., Bd. 3.

1889 Beitriige zur Entwickelungsgeschichte des Saugerthierherzens.

Arch. f. mikr. Anat., Bd. 33. Favaro, G. 1913 Ricerche embriolog. ed. anatom. intorno al cuore dei verte brati, Pai'te I. Padova. His, W. 1885 Anatomie menschlicher r]mbryonen. III. Zur Geschichte dei*

Organe. Leipzig. HocHSTETTER, F. 1901-1903 Die Entwickelung des Blutgefiisssystems. Hert wig's Handbuch der vergleich. und experim. Entwickelungslehre der

Wirbeltiere. Bd. 3, 1906. Lewis, F. T. 1903 The gross anatomy of a 12-mm. pig. Am. Jour. Anat.,

vol. 3. Morrill, C. V. 1915 A preliminary note on the septum secundum in the pig.

Anat. Rec, vol. 9, p. 111. Retzer, R. 1908 Some results of recent investigations on the mammalian

heart. Anat. Rec, vol. 2, p. 149. Rose, C. 1888 Beitrage zur Entwicklungsgeschichte des Herzens. Dissert.

inaug. Heidelberg.

1889 Zur Entwicklungsgeschichte des Saugerthierherzens Morph. Jahrb., Bd. 15.

1890 Zur Vergleichenden Anatomie des Herzens der VVirbelthiere. Morph. Jahrb., Bd. 16.

Tandler, J. 1912 The development of the heart. Keibel and Mall's Manual of Human Embryology.

1913 Anatomie des Herzens. Bardeleben's Handbuch der Anatomie des Menschen Bd. 3, Abt. 1.

Thyng, F. W. 1911 The antomy of a 7.8 mm. pig embryo. Anat. Rec, vol. 5.

1914 The anatomy of a 17.8 mm. human embryo. Am. Jour. Anat., vol. 17.




5 Reconst ruction of the heart of a 7.9 mm. embryo. The right atrium and right ventricle have been opened fi'om the right side, the cut passing through the junction of the transverse part of the sinus venosus {Sn.t.) and the right sinus horn (Sn.d.). Magnified 25 diameters.

6 Reconstruction of the heart of a 15.2 mm. embryo, thd right atrium and right ventricle opened from the right side. Magnified 25 diameters.


A., Aorta dorsalis

Ao., Aorta (ventral part)

A.d., Atrium dextrum

A.S., Atrium sinLstrum

Bulb., Bulbus cordis

Cr.ter., Crista terminalis

En.s., upper endocardial cushion

End., lower endocardial cushion

En.c, fused endocardial cushions


L.V., Limbus fossae ov

O.I, Ostium primuin

O.II, Ostium st'cuiulun

O.iu., Ostium intorvcn

Per., Pericardium

S.I, Septum primum

S.II, Septum secundum, Septum interventriculare

Sn.t., Sinus venosus, trans, part

Sn.d., Sinus venosus, right horn, sinus septum

s (Vieussenii)

Sn.cor., Sinus coronarius, Spatium intersepto-valvulare, Sulcus interventricularis T.vv., Tensor valvulae = Septum spu rium Vv.v., Valvulae venosae V.v.d., right valve V.V.S., left valve V.f.o., Valvula foram. ovalis, right com. card, vein, left com. card vein V. car. a.d., right ant. card, vein, right post, card, vein V.C.S., Vena cava superior V.C.I. , Vena cava inferior, Vena azygos V.scL, Vena subclavia V.h., Vena hepatica X, (fig. 9)= part of right sinus valve

guarding coronary orifice



7 Reconstruction of the heart of a 21.0 mm. embryo. The right atrium and right ventricle have been opened from the right side, the cut passing through a part of the coronary sinus (Sn.cor.). Magnified about 25 diameters.

8 Same as figure 7 but in slightly different position. The right sinus valve (V.v.d.) has been partly cut away, exposing the orifices of the coronary sinus and inferior vena cava. Probes have been inserted in the superior and inferior cavae and the coronary sinus. The probe in the coronary sinus passes across the sinus septum { under the right valve. Magnified about 25 diameters.



9 Dissection of the heart of a foetus of about 85 mm., the right atrium and right ventricle opened from the right side. The lateral wall of the inferior vena cava (V.c.i.) and the right sinus valve (V.v.d.) have been divided by a vertical cut and the parts somewhat separated. Magnified about 10 diameters.

Cite this page: Hill, M.A. (2024, February 24) Embryology Paper - On the development of the atrial septum and the valvular apparatus in the right atrium of the pig embryo (1916). Retrieved from

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