Talk:Paper - On the development of the superficial veins of the body wall in the pig (1909)

On The Development Of The Superficial Veins Of The Body Wall In The Pig

Helen Willlston Smith. From the Anatoiiiivul Lahoratonj of the Johns Hopkins University.

With 11 Figures.

Satisfactory studies of the vascular system of young embryos have been impossible until quite recently, for the embryologist has been unable to see much more than mere fragments of the growing ends of this system in embryos treated by the usual methods of preparation. During the past few years the method of injection of the vascular system of young embryos has been perfected more and more in this laboratory, so that now we are able to procure complete injections in the very youngest stages. In order to make proper headway in the study of the morphology of the vascular system it is necessary to study the development of the primitive vessels in the embryos. For instance, more fundamental conditions can be obtained for the study of development in the umbilical vein, than in the vessels of an organ ; in the former case there is but one vessel to be followed, while in the latter there are millions, and it is practically impossible to find the same terminal twig from stage to stage.

The key to the situation is obtained when the main trunks and all their branches are brought out sharply by means of injection in their very earliest and in subsequent stages. This has now been accomplished by a number of investigators in this laboratory, most successfully, probably, by Dr. Evans, who injected many of the embryos I have studied.

In order to obtain perfect injections it is necessary to inject live embryos, and, in addition to tadpoles and chicks, an abundance of The American Jouknal op Anatomy. — Vol. IX, No. 3.

440 Helen Williston Smith.

pigs of various stages of development are available every day. In the latter case the injection of India ink is made into the umbilical artery towards the heart which, while beating, enables one to obtain perfect injections.

Studies in this laboratory have shown conclusively that the entire vascular system is developed from a common plexus of capillaries which gradually extends over the whole body, a part of which is transformed into arteries and a part into veins. Throughout development the vessels are functioning, and the formation of arteries and veins is only an expression of the law of functional adaptation of the extensive capillary plexus peripheral to a beating heart. How could it be otherwise, for the arteries and veins are not formed step by step by sjorouts, or by the union of independent anlages, but they are functioning from the time of their simplest beginning until the animal dies.

The present study was undertaken, at the request of Dr. Mall, in order to follow, in a relatively simple field, the gradual evolution of the vascular system from its first appearance until its adult form is reached. This study is one of a series, two of which by Dr. Evans are now in press, and others are in preparation. If circumstance will permit I hope to follow this with an account of the development of the deeper vessels of the body wall.^

We find in the earliest stages considered in this jiaper a relatively simple circulation in the body wall, one in which the posterior cardinal and the umbilical veins are both formed, but have comparatively few ramifications. As the embryo grows the limb buds appear and the membrana reuniens closes in around the umbilical

'The literature on the standpoint taken in tliis study is as follows : Aeby, Der Bau des menschl. Korpers, 1871; Baader, Inaug. Diss., Bern, 1866; Ttioma, Untersuch. iiber die Histogenese und Histomecbanik des GefJisssystems, 1893; Flint, Johns Hopkins Hospital Reports, IX, 1900, Amer. Jour. Anat., II, 1903, and VI, 1907 ; Mall, Amer. Jour. Anat., IV., 1905, and V, 1906 ; Rabl, Arch. f. m. Anat., LXIX, 1907; Evans, Anatomical Record, II, 1908, and Amer. Jour. Anat., IX, 1909.

The specimens on which the present article is based were demonstrated at the last meeting of the Association of American Anatomists, Baltimore, Decemlier, 1908.

Superficial Veins in the Pig. 441

cord. The posterior cardinal and the umbilical veins share in draining the limb buds, one dorsally, the other vcntrally, and the umbilical drains as well a plexus which forms in the membrana reuniens. As the posterior cardinal vein sinks into the depth, though it continues to partly drain the limb buds and to receive its segmentals from the myotomes, the relatively vast area of the membrana reuniens drains entirely into the umbilical vein. Then, as the plexus in the membrana increases in complexity and the muscle layer shifts into it ventrally, larger longitudinal anastomoses form along the body wall draining up under the anterior limb bud to the vessels there, which connect in turn with the cardinal veins. Soon a definite vessel is formed, the thoraco-epigastric, which increases rapidly in size until it collects to itself almost all the tributaries of the umbilical vein. The plexus in the membrana reuniens, in consequence, gradually dies out until only a few vessels in the median line and in the lower ventral region remain. Meanwhile on the mesial side of the muscle layer and ribs, other vessels, namely, the internal mammary and the deep epigastric veins and arteries have been formed from a longitudinal plexus, and the intercostal vessels have been spun out like strands of cobweb in the intercostal spaces. All these vessels not only anastomose among themselves, but also have very numerous communications with the superficial vessels. Finally, it comes about, by changes given in detail later, that the thoraco epigastric loses its axillary connections, and drains into the internal mammary. After this the vessels of the body wall are not changed in kind, but in degree only, and the condition of the adult is practically achieved.

Turning to the literature concerning the development of the superficial blood vessels of the body wall, we find a number of observations upon the subject, but these are given, in great part, either as isolated or unexplained steps, or in an attempt, more or less satisfactory, to exjDlain the condition in the adult. These latter observations, for the most part, are made upon fcetuses, and so only a clue can be gleaned here and there concerning the early development. Among observations upon very young embryos are those of Coste, Kolliker, His, and Mall.

442 Helen Willistoii Smith.

His describes a human embryo in which the membrana reiiniens contains vessels emptying into the sinus reuniens above, and into the umbilical vein below. This is a condition found in pig embryos of about 7 mm. and one that is easily interpreted by a study of younger and older stages. This observation is confirmed and extended by Mall, who says, 'Tt appears, then, that during the third week of development, while the umbilical veins still empty into the sinus reuniens, an extensive plexus is formed throughout the greater extent of the membrana reuniens, which receives blood from the aorta on its dorsal side, and empties into the umbilical vein on its ventral side. As the umbilical vein changes its position to enter the liver, this circulation through the membrana reuniens is broken up as a much earlier circulation through the umbilical vesicle was broken up."

Kolliker and Coste give a description of a somewhat older type. Kolliker pictures a cow's embryo in which the membrana reuniens is filled with a minute plexus radiating from the myotomes to the umbilical vein, and Wertheimer quotes Coste as follows, speaking of the vessels in the abdominal wall of the adult: "Ces vaisseaux sont les restes du riche appareil veineux transitoire, qui des parois abdominales sur lesquelles ils etaient repandus, se portent vers la veine ombilicale ou allantoi'dienne droit dans laquelle ils penetrent par une foule de troncs, place les uns a cote des autres. Ils suivent la destinee de la veine qui les regoit et s'eteignent completement avec elle."

That I am correct in naming the vessel described above as the thoraco epigastric is evident upon comparison with the thoraco epigastric in the human adult. This is a vein subject to considerable variation, and described somewhat differently in the text-books. Toldt and Spalteholz and Piersol describe it as extending subcutaneously from the superficial epigastric vein, on the anterior and lateral surface of the trunk, to enter the long thoracic. Sabotta says it may either enter the long thoracic or the axillary vessel directly. In this laboratory I have examined a number of cadavers which show variations, agreeing for the most part with the two types given by Sabotta. The thoraco epigastric vein is unques

Siiporficinl Veins in the Pig. 443

tionably the same as that described by F. T. Lewis in rabbit embryos, and called by him the external mammary vein. (Amer. Jour. Anat., 1906.)*

In general we may say that the thoraco epigastric is a vessel connecting the veins of the epigastric plexus with the axillary veins. This is exactly the condition of the vein in the pig embryo of about 20 mm., and though in the adult we find it has undergone further change, enibryologieally it must be regarded as the same vessel.

Joris, after speaking of this same stage, says, "II est done un moment ou les veins umbilicales representent les seul troncs collecteurs des vaisseaux parietaux, enfin, les veines parietales perdent leur troncs collecteurs par I'atrophie de la partie superieure des veins ombilicales, et finissent par se rattacher au systeme veineux cave." There is never a time in the embryo pig in which the umbilical vein drains the whole body wall, taken in a broad sense to include the limb buds, but it is certainly the chief collecting vessel for a considerable period. Finally the vessels emptying into it do atrophy, as the blood flowing from the body wall is directed into the cardinal veins. The method by which this is effected is, as I have said, chiefly through the development of the thoraco epigastric vein, the description of the origin, growth and permanent condition of which gives the connecting links between stages in the embryo and those of the adult.

Concerning the adult condition in man, especially in the ventral body wall, much has been written, and though an account of that literature does not come strictly within the bounds of this paper, it may be of interest to give a brief resume of it here. It deals chiefly with the question whether or not the umbilical vein remains patent, and the various points of communication between the portal and systemic circulation. There is considerable difference of opinion, due perhaps to the different methods of attack upon the problem, and to the great amount of anatomical variation which unquestionably must exist.

Since this article went to press Dr. Lewis has also adopted the term thoraco epigastric. Anier. Jour. Anat., Vol. IX, No. 1, Feb., 1909.

444 Helen Williston Smith.

The names chiefly associated with this work are those of Robin, Baumgarten, Wertheiraer, Sappey, Burow, Pfeifer, His, and recently Joris.

I have not seen Robin's papers, but he is quoted by most of the other authors, generally with more or less indignant sorrow because of the incorrectness of his views, namely, that the umbilical vein never receives vessels from the abdominal wall in the fdtus, and is completely obliterated after birth.

Baumgarten, on the other hand, according to Pfeifer and Joris, admits the existence of collateral veins in the adult, describes their arrangement as constant and normal and says that the part of the umbilical vein remaining patent is connected with the deep epigastric veins.

Wertheimer comes to the conclusion, from injections of thirteen foetuses and young infants in the hepatic extremity of the umbilical vein, that ordinarily the umbilical vein becomes absolutely occluded. However, there is a venule of later formation running in the obliterated cord in the adul't, and he admits that cases may exist in which the umbilical vein remains oj^en permanently. This possibility he explains by reference to comparative anatomy, for in amphibians the umbilical vein persists as the anterior abdominal vein.

Sappey is somewhat more positive than Wertheimer in stating that the umbilical vein is absolutely occluded in the adult, but he says accessory veins exist, which he divides into a superior and an inferior group.

"Le gi-oupe superieur est constitue par des veinules que descendent de la partie mediane du diaphragme vers la face convexe du foie et qui viennent se distribuer sur les lobules auxquels adhere le ligament suspenseur. Par une de leurs extremites, ces veinules communiquent avec les veines diaphraginati(]ues, et par 1' autre avec les divisions sus-lobulaires de la veine porte.

"Le groupe inferieur comprend toute une serie de veinules qui se portent de la partie sus-ombilicale de la parol abdominale anterieure vers le sillon longitudinal du foie. Ces dernieres, comprises dans la partie du ligament suspenseur qui renferme le cordon de la

Superficial Veins in the Pig. 445

veine ombilicale, se trouvent en communication, a leur origine, avec les veines epigastriques et les veines tegumenteuses de I'abdomen."

Burow describes a vein formed from the union of branches from the right and left epigastric. This vein passes up towards the liver and enters the upper part of the umbilical vein. Joris maintains that this vein is the same one as that described by Sappey, with the difference that in the one case the vein enters the liver, and in the other enters the unobliterated portion of the umbilical vein just before it reaches the liver. He says, moreover, that the right as well as the left umbilical vein may persist in the adult as a communication between the liver and the right epigastric vein. His work was done by injecting the portal vein after ligature of the vena cava above and below" the liver. These injections were made on foetuses two months old and older, and on a few infants.

His has made a classification of these veins as follows:

"(1) W parumbilicales (Sappeyi) welche von der Nabelgegend aus zur Leber emporsteigen und in deren Substanz sich einsenken. .

^'(2) V supra umbilicalis (Baumgarten's Burowsche Vene) welche in das obere, offen gebliebene Ende der V. umbilicalis einmiindet.

(3) W umbilicovesicales. (Braunes' Burowsche Venen.)

"(4.) W umbilicoepigastricae, welche beiderseits in die W epigastricae inferiores profundae einmiinden."

Summing up these observations it seems evident that ordinarily there are some small venules running from the region of the diaphragm to the umbilicus, and that these connect the portal system with small branches of the deep epigastrics.

In pigs about three centimeters, in which all the vessels of the membrana reuniens appear to have atrophied, sections show that small vessels pass from the liver in the median line to the umbilical vein, and that there are also some twigs connecting the umbilical vein with the plexus in the region of the epigastric veins. However, from a study of the vessels of the membrana reuniens in younger embryos it is evident that the probability of variation is great which naturally complicates studies of this kind very much.

The smallest injected embryo considered here is one about 6 mm. (Fig. 1). It may be noted that this specimen is twisted upon

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itself through a considerable angle. This twisting is probably not normal, but it permits of a very good view of the blood vessels, and this embrvo has therefore been selected for illustration. The strik

FiG. 1. — Embryo 6 mm. long. Enlarged 17 times.

Cor, heart ; V.o, omphalomesenteric vein ; Ao, aorta ; Y.cps, left posterior cardinal vein; V.us, left umbilical vein; Y.ud, right umbilical vein; V.cas, left anterior cardinal vein ; V.cpd, right posterior cardinal vein ; A.om, omphalomesenteric artery; A.ns, left umbilical artery.

ing thing about it is the extreme simplicity of its vascular system. The aorta is large. It gives off a number of spicule-like vessels, many of which on the ventral side unite to form the omphalo

Superficial Veins in the Pig. 447

mesenteric artery, a conspicuous, bulky vessel that increases in size as it passes anteriorly. Just below the omphalomesenteric artery the aorta divides into two vessels which in turn break up into two groups of capillaries, each of which reunites to form an umbilical artery. In the head region there are only two branchial arches formed. From the anterior of these a branch is given off which passes into the capillaries that unite to form the anterior cardinal vein (V. cas.). The anterior cardinal vein runs back to meet the posterior cardinal (V. cps.) and the two form a plexiform union before they enter the heart together. The posterior cardinal cannot be traced below the mesonephros, but it is possible that the injection is incomplete as in embryos a very little older than this it extends dorsally to the posterior limb bud. The umbilical veins are plainly visible, running from the allantois along the edge of the membrana reunions to the sinus reuniens which they enter together with the omphalomesenteric veins. (Vv. om.) These vessels are not clean cut, but show clearly their plexiform origin. Along the left umbilical particularly, we see many loops and openings. There are also some spicule-like projections here and there along the course of the umbilical veins that form the anlage of the future plexus of the membrana reuniens.

The second embryo, 7 mm., pictured here in Fig. 2, corresponds roughly, as I have said, with that described by His. Probably the most striking thing about it is the size of the umbilical veins (Vvu). In the figure the right vein is seen to run from the cord in a long curve for the whole length of the mesonephros to the liver. At a point very little below the liver, a relatively small vein is seen looping up superficially and emptying at the anterior portion of the liver into the sinus reuniens (SR) above. This vessel is a part of the umbilical that does not sink into the depth, and receives numerous tributaries from the arm bud. The arm bud, however, drains also into the posterior cardinal vein (Vcp) above, and below by five good connections, directly into the large umbilical vein (Vud). Below these connections, until the posterior limb bud is reached, there is, as yet, only a very narrow strip of body wall to drain. Such few vessels as there are here run into the

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Helen Williston Smith.

posterior cardinal (Vcp), but lower down there is a very rich plexus, lying ventral to the anlage of the posterior limb bud, which communicates freely with a similar plexus on the opposite side of the

Fig. 2. — Embryo 7 mm. long, in wliicli the injection is complete. The vessels in the head are semi-diagrammatic. Enlarged 21 times.

Y.lf, linguo facial vein; SR, sinus reuniens ; V.nd, right umbilical vein; vein; V.iis, left umbilical vein; A.om, omphalomesenteric artery; Ao, aorta; V.ca, anterior cardinal vein ; V.cj), posterior cardinal vein ; Pars sup. V.u, superficial part of umbilical vein.

body, and as the figure shows, with its respective umbilical vein. Dorsal to the posterior limb bud the posterior cardinal (Vep) arises from numerous, capillaries which unite to form a vein running along

Superficial Veins in the Pig. 449

the body wall. This receives some small veins and finally sinks into the dei:)th under the anterior limb bud, receives two or three twigs from it, and uniting with the anterior cardinal (Vca) enters the sinus reunions in a graceful, sweeping curve. The sinus reunions also receives a vein, the inferior jugular, formed by the union of a number of capillaries which rise in gill arches, where they anastomose with twigs to the anterior cardinal. The veins that form the anterior cardinal (Vca) are very large and striking, particularly the one which curves in a half circle above the anastomosing tips of the cervical segmental arteries to enter the anterior cardinal. A chain of anastomoses along the spinal cord, formed from the tips of the segmental arteries passes from the region of the head to a point below the anterior limb bud. This plexus drains back into the posterior cardinal vein through its segmentals. The aorta is enormous. Three aortic arches are showii. The most anterior of which is not well injected. The omphalomescntpric artery (Aom) is represented by four vessels which unite at some little distance from their origin. In the tail the aorta divides into two vessels which anastomose at the tip.

The next embryo, Fig. 3, is a very little larger than that just described, the chief point of difference being the presence of a thick capillary mesh in the membrana reunions.

As before, there remains 'a superficial part of the umbilical vein (Vud) draining the posterior limb bud, which also drains largely into the posterior cardinal vein. The limb bud contains a fine plexus of veins which tend to form a border vein, while dorsal to it the welldeveloped mesh runs out upon the body wall to unite with the general plexus of the membrana reunions. The plexus of the membrana reunions is evidently the same as that described by Coste. It is very characteristic of the membrana, being made up of comparatively large vessels anastomosing among themselves, but for the most part passing very directly to the umbilical ' vein which they enter by parallel veins.

The next embryo in the series. Fig. 4, shows these vessels even better developed, since the membrana has progressed farther. It represents most completely the phase in the body wall when it drains

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Helen Williston Smith.

chiefly into the umbilical vein. The lower part of the membrana reuniens (MR) as high as the point where the umbilical vein enters the liver, is seen to be full of veins. These rise from a fine network of capillaries which is fed by the segmental arteries and extends

Fig. 3. — Embryo 8 mm. loug. Enlarged 14 times.

Only the superficial vessels are shown.

Vlf. linguo-facial vein; 8R. sinus reuniens ; Pars sup. V.u, superficial portion of umbilical vein ; MR, membrana reuniens ; V.ud, right umbilical vein ; V.ca, anterior cai'dinal vein ; V.cp, posterior cardinal vein.

in a crescent shape, with the concavity directed ventrally between the two limb buds. In the lower portion, this network is entirely irregular, but higher up it forms a more or less connected plexus which passes partly into another plexus extending ventrally to the

Superficial Veins in the Pig.

451

anterior limb bud out towards the region over the liver, and partly, into two distinct, though very fine ropes of capillaries running up under the anterior limb bud, the more dorsal of which is the anlage of the thoraco epigastric vein (Vte). Over most of the

Fig. 4.— Embryo 10 mm. long. V.te, thoraco epigastric vein ; vein.

Enlarged 1.3 times.

MR, membrana renniens;

Vu, umbilical

upper part of the membrana there are no blood vessels visible and the superficial part of the umbilical vein, shown in Figs. 2 and 3, appears to have atrophied. When compared with Fig. 5 it is evident that the system draining into the umbilical vein is receding and giving place to one draining longitudinally between the limb buds.

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Helen Williston Smith.

Plexa6 Yes

Fig. 5.— Embryo 15% mm. long. Enlarged 10 times. A few vessels in the deptli are dotted.

V.m, border vein; MR, membrana reuuieus ; V.te, thoraco epigastric vein; Ves, superficial epigastric vein; V.u, umbilical vein.

Superficial Veins in the Pig. 453

There are still many blood vessels in the membrana (MR), but they show a tendency towards atrophy. The thoraco epigastric (Vte), on the other hand, which in the previous figure (Fig. 4) was nothing but a thread of capillaries, in Fig. 5 shows as a very distinct vessel passing up under the limb bud, receiving the primitive ulna, and running on up to enter the posterior cardinal at its junction with the anterior cardinal. The central connections of the thoraco epigastric, in this figure, show very well, but the picture is not always so uncomplicated. It will be noticed that the vein runs dorsal to the artery while in the adult it is normally ventral. The change is effected as follows. There is at the root of the arm bud a capillary mesh surrounding the artery connected above with the cardinals at their junction and below with the jtrimitive ulnar. In young stages the dorsal portion of this capillary mesh or loop is often the more prominent, but, later, the blood tends to take the ventral short cut and the dorsal part astrophies. The thoraco epigastric may be looked upon as a continuation of this mesh extending out upon the body wall. It drains a small area, below and dorsal to the limb bud and has numerous connections with the capillaries supplying the lower part of the membrana reunions. These latter capillaries, it will be noticed, show a tendency to form into a long ropelike plexus, running from the region ventral to the posterior limb bud up towards the anterior limb bud. This rope of capillaries later forms the superficial epigastric (Ves) and may therefore be considered as part of the permanent type.

That the injection over the heart of this embryo is not complete is very probable because sections of this same stage show injection all over the upper heart region. This is shown in Fig. 6. Here, on either side of the U-shaped aortic arches, we find good-sized veins that empty into the internal jugulars (Vji). These veins drain the upper part of the membrana over a bib-shaped area, somewhat greater than is shown in the section, and anastomose on the sides with veins that enter the posterior cardinal at its junction with the anterior cardinal. Fig. 7 is from a section of this same embryo at the level of the omphalomesenteric artery and shows the way in which the blood is supplied to the muscle layer and to the body wall. The

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paired segmental arteries are seen passing out at a wide angle from each other, and each breaking up into a tuft of vessels, twigs of which run into the inner and outer side of the muscle layer and to the anterior spinal artery and cord. These twigs pass into fine capillaries which may then be traced into the veins. The venous blood is car

FiG. 6. — Section one-half millimeter thick of an emhryo 15i/^ millimeters long.

MS, spinal cord.; V.ji, internal jugular vein ; 'T, trachea ; Aa, fourth aortic arches; MR, membrana reuniens.

ried oif in one of three ways. Either it may run through the thoraco epigastric to the posterior cardinal, or it may run into the membrana to the umbilical vein, or it may run back through the dorsal segmental veins into the mesonephros to the posterior cardinal veins (Vcp). The sections of this embryo also show that at this stage the internal mammary vein and artery are not present, as such, but that

Superficial Veins in the Pig.

455

the capillaries on the mesial side of the muscle layer have a tendency to unite and knot together to form a chain, the upper end of which runs into the posterior cardinal. The artery is represented by a few fine capillaries which run from the subclavian artery out under the arch of the thoraco epigastric.

V. Plexus MR

Fig. 7. — Section one-fourth of a millimeter thick of an embryo 15% mm. long ; taken just below omphalomesenteric artery.

MS, spinal cord ; Vtc, thoraco epigastric vein ; Ao, aorta ; Vv.cp, posterior cardinal veins ; V. plexus MR, veins of the plexus of the membrana reuniens ; A.om, omphalomesenteric artery ; Yais, left umbilical vein ; V.ud, right umbilical vein ; M, mesonephros.

From this stage on, however, the internal mammary vein and artery as well as the thoraco epigastric and the plexus of the superficial epigastric developed rapidly. This further development is seen in Fig. 8. The thoraco epigastric (Vte) and superficial epigastric plexus (Ves) are now draining practically all of the dorsal side of the muscle layer of the body wall which has grown considerably farther

-Plexu5 v.es

Fig. 8. — Embryo IS mm. long. Enlarged 12 times.

Only most superficial vessels are shown.

V.te, thoraco epigastric vein ; V.mi, internal mammary vein ; MR, membrana reunions; Plextis V.es, plexus of superficial epigastric vein; V.u, umbilical vein.

Superficial Veins in the Pig. 457

forward carrying the blood vessels with it. The internal mammary (Vmi) is represented in the figure by a straight line ventral to the thoraco epigastric (Vte). It lies on the mesial side of the muscle layer and has very numerous capillary connections with the thoraco epigastric. Posteriorly it anastomoses with the plexus of the deep epigastric, which runs beneath the superficial epigastric and is not shown in the drawing. The membrana reuniens is still large and well supplied with blood vessels, though it is evident that less blood runs from the body wall to the unbilical vein than formerly. As the internal mammary and thoraco epigastric veins now lie, their paths to the heart are about equal in length, and it is natural therefore that blood supplied to the outer side of the muscle layer should pass back through the thoraco epigastric and that to the inner, through the internal mammary. It is evident, however, that, as the muscle layer grows forward, it will carry with it the internal mammary. The thoraco epigastric being an axillary vessel must still continue to empty into the axilla and therefore were the lower part of the vessel carried forward, the course of the blood through it, on the outer side of the muscle layer, would become more round about than that through the internal mammary. It is therefore to be expected that the blood, following the path of least resistance, will tend to flow from the lower part of the thoraco epigastric through the numerous connections into the internal mammary and that, these vessels enlarging in consequence, the path to the internal mammary will become so easy that practically all the blood from the lower outer body wall will pass that way. This is what proves to be the case. In embryos about 18 or 19 mm. long the thoraco epigastric, as such, reaches its maximal development. Then it drains practically all the outer body wall between the limb buds, back as far as the circulation connected with the spinal cord, while ventrally it receives vessels from the membrana and anastomoses very frequently with the superilcial epigastric and with the internal mammary. These anastomoses grow larger so that while the more posterior part of the thoraco epigastric becomes practically continuous with the superficial epigastric, anteriorly it begins to drain largely into the internal mammary. At this latter point a characteristic elbow is usually formed from which, as is

Fig. 9. — Embryo about 3 cm. long. Enlarged 6 times.

All vessels except tbose immediately conuected with the thoraco epigastric vein are omitted.

Pars axillaris V.te, axillary portion of thoraco epigastric vein; Vv. et a.mi, internal mammary veins and artery; V.te, thoraco epigastric vein; MR, membrana reuniens; A.ep, deep epigastric artery.

Superticial Veins in the Pig. 459

shown in Fig. 9, vessels pass to the internal mammary. Only one of these persists in older stages. There are all manner of variations as to the proportion of the thoraco epigastric that is left draining into the axilla. Sometimes almost the whole vessel is taken over completely and sometimes, as in Figure 9, a considerable portion is left. This figure shows very well the transition stage of the thoraco epigastric. The vessel is seen passing on along the edge of the muscle layer to a point where a fan-shaped plexus of vessels conceals its anastomoses with the internal mammary. Here it swings in a long loop back to its axillary connection. This loop is, however, noticably smaller than the vessel below the turn, and it is evident that a good deal of the blood has already been deflected into the internal mammary. This connection with the internal mammary is jjlainly shown in the next figure. (Fig. 10). It also shows how far the internal mammary has developed (AmiVvmi), that it is now a double vein with the artery running between, receiving anterior intercostal veins, which anastomose with the intercostals proper. It also receives a great many fine, anastomosing vessels, which have been dissected away from the upper part of the membrana reunions. The membrana is still of considerable size but the blood vessels are of a very feeble type compared with the earlier ones, and drain almost entirely back to the body wall through the superficial and deep vessels. As the membrana grows smaller and smaller, the blood vessels on the surface atrophy until only those along the edge of the advancing muscle layer are left visible. This is shown in figure 11, which is from an embryo 3 cm. long. This embryo illustrates chiefly, however, a case where almost all the thoraco epigastric along with the superficial epigastric with which it forms a continuous vessel, drains into the internal mammary. The internal mammary has been carried forward, while the stump of the thoraco epigastric has been left well back in the axilla. This is a very typical case. The chief variation being, as I said before, in the proportion of the thoraco epigastric taken over to the internal mammary. As the membrana continues to recede, and the muscle layer advance, the internal mammary vessels are carried nearer together and along with them the superficial veins, so that ultimately we find the transferred portion of the

Fig. 10. — Embryo 3 cm. long. Enlarged about 5 times.

The anterior limb is removed.

Pars axillaris V.te, axillary portion of tboraco epigastric vein; Vv. et a.nii. internal mammary artery; Vv.mi, internal mammary veins; MR, membrana reuniens; V.te. tboraco epigastric vein; A.cp, deep epigastric artery.

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VvelQ.ml

V.te

pi^'

MR

A.ep

Fig. 11. — Embryo 3 cm. long. Enlarged 6 times.

Pars axillaris V.te, axillary portion of thoraco epigastric vein ; Vv. et a.mi, internal mammary artery and veins; V.te, thoraco epigastric vein; MR, membrana reuniens; Aep, deep epigastric artery.

462 Helen Williston Smith.

thoraco epigastric as a very superficial vessel that may be seen plainly in uninjected specimens, running from its forked origin near the hind leg, along the milk ridge up to the manubrium at which point it dips sharply down to enter the internal mammary vein. This completes the history of the changes in the superficial blood vessels of the body wall.

During this development, four circulations obtained in the superficial layers. First, the circulation in which the posterior cardinal plays a part. Second, the circulation across the membrana reuniens to the umbilical vein ; then, thirdly, the formation and growth of the thoraco epigastric and superficial epigastric on the outer side of the muscle layer; and somewhat later, that of the internal mammary veins and artery on the mesial side. The thoraco epigastric grows with the superficial epigastric until they drain the whole superficial body wall dorsalwards as far as the spinal cord. Meanwhile the internal mammary vessels have grown. The intercostal veins and arteries also have been spun' out of the plexuses of the segmental vessels, as the muscles and ribs invade the membrana reuniens, and they anastomose with the anterior intercostals from the internal mammary vessels. The internal mammary vein increases in size. Its connections with the thoraco epigastric increase also, and gradually the end of the thoraco epigastric is switched off, and we reach the fourth and final stage in which the superficial body wall drains largely into the internal mammary vein. After this condition is reached further change is not so much in kind as in degree.

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Balfour. F. M. Comiiarative Embryologj', II, 658.

BUKOW. Archiv f. Aimt. ii. Pliys., 183S, S. 44.

EcKER n. WiEDERSnEiN. Anatouiie cles Frosches, S. 413.

His. Auat. inensch. P^uilu-youeii. Ill, S. 20B. also Fig. 130.

His. Die anat. Noinenclatur. Leipzig, 1895.

JoRis. Rechercbes sur les Veines Ombilicales et Para Ombilicales. Bull.

de I'Acad. Royale de Medeciiie de Belgique, 1905. KoLLiKER. Grundriss d. Entwickl. d. Meuscben, S. 103. Fig. 58, 1884. Mall. Journal of Morpbology, XIV. p. 362, 1898. Pfeifer. Zur Keuntnis des bistolog. Baues und der Riickbildung der

Nabelgefiisse und des Duet. Bot. Arcb. f. Patb. Anat.. CLXVII. Sappey. Veines portes accessoires. Jour, de I'Anatomie, XIX, 1883. Wertheimer. Recbercbes sur la veine onibilicale. Jour, de I'Auat. et de la

Pbys., XXII. 1886.