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=The Relative Role Played By The Embryonic Veins In The Development Of The Mammalian Vena Oava Posterior=

Elmer G. Butler


Laboratory Of Comparative Anatomy, Princeton University

Twenty~Six Figures

==Introduction==
This research is the direct outgrowth of those investigations which have preceded it on the development of the posterior vena cava in the cat by Huntington and McClure (’07, ’20) and in man by McClure and Butler (’25). Their study of closely graded developmental stages has revealed hitherto unrecognized factors involved in the formation of the posterior vena cava and has established a detailed knowledge of the ontogeny of this vein in these mammals. Such knowledge leads directly to a broader ﬁeld and more comprehensive problem, namely, the development of the posterior vena cava in mammals in general and to a consideration of the primary developmental factors, so far as they can be determined, which inﬂuence and govern its formation. The central aim, therefore, of the present investigation has been to make a careful study, by the method of comparative embryology, of the relative functional role played by the various embryonic veins associated in the development of the mammalian posterior vena cava.

I acknowledge with pleasure my sincere gratitude to Prof. Charles F. W. McClure, at whose suggestion this investigation was undertaken, for his aid and advice throughout the course of the work. My thanks are also particularly due to Prof. George S. Huntington for full access to the Embryological Collection of the College of Physicians and Surgeons of Columbia University and for his kindness in allowing the use of several wax reconstructions. In addition, my thanks are due to the following gentlemen: to Prof. Frederic’ T. Lewis for access to the Harvard Embryological Collection and for the loan of embryos for use at Princeton; to Prof. Bradley M. Patten for the loan of series LXIV and series 263 B from the Embryological Collection of the Western Reserve University School of Medicine, and to Dr. E. L. Shaffer and to Mr. E. M. Shearer for the use of several wax reconstructions made by them in the Princeton laboratory.

HISTORICA L ACCOUNT

A complete resume of the literature concerned with the development of the posterior vena cava in mammals cannot be attempted within the limits of the present paper, for no other single vein has been the subject of research so extensive or has associated with it so large a bibliography. Among the investigations which have contributed to our present knowledge of the embryology of this vein, those of Rathke (’32, ’38), Hochstetter (’93), F. T. Lewis (’02), and Huntington and McClure (’07, ’20) are preeminent. A brief consideration of the contributions of these investigators will serve to acquaint the reader with the main facts associated DEVELOPMENT on THE POSTERIOR VENA CAVA 269

with the problem and with the purposes governing the present study. For more complete accounts of the earlier investigations, one should refer to the historical reviews of Kerschner (’88), and of Hochstetter (’93), and to the original papers themselves.

Rathke, in his papers of 1830 and 1838, based on a study of sheep embryos, laid the foundation for our present knowledge concerning the embryology of the venous system in mammals. In his earlier work Rathke (’30) held that the right posterior cardinal vein, which from the time of its appearance he called the right posterior vena cava, became transformed throughout its entire length into the adult vena cava. Later, however, in his better-known work, Rathke (’38) abandoned entirely this conception and, inﬂuenced probably by the observation of Stark ( ’35) that the proximal portion of the vena cava came from a portion of the omphalomesenteric vein within the liver, advanced an entirely different theory regarding the method of development.‘ According to this later account, the posterior vena cava arose as a single unpaired vessel throughout its entire length. He described it as a new channel growing posterior from the liver, passing medial to the mesonephroi, and ﬁnally joining with the caudal ends of the posterior cardinals at the level of the iliac veins. During its growth caudad it received tributaries from the mesonephroi and sex glands. Rathke’s essential idea was that the cava originated as a vessel entirely independent of any preexisting venous channels, and that the posterior cardinal veins contributed not at all to its formation.

The researches of Hochstetter on the venous system of the vertebrates, extending principally over a period between 1888 and 1893, are too well known, both from the original papers and from text-book accounts, to justify anything but a brief consideration. In the case of mammals, his most extensive observations were made on embryos of the rabbit. Hochstetter’s conception was that the posterior vena cava developed downward from the liver by Way of the caval mesentery and then extended along the "medial side of the 270 ELMER G. BUTLER

right mesonephros, while a similar vein, medial to the left mesonephros, connected with the cava by several cross anas— tomoses at the level of the omphalomesenteric artery. Later, this system acquired a connection at this same level with the cardinal vein on each side, and eventually the right posterior cardinal vein, caudal to this point of connection, became the adult posterior vena cava. The location of the adult Vena cava medial to the right kidney and ureter came about by a split in the posterior cardinal vein; this gave rise to a perinreteric venous ring, the lateral half of which was lost, while the medial portion persisted as the main channel. Hoch— stetter’s diagrams for the rabbit have enjoyed wide popularity and are familiar to all students of embryology. The essential point emphasized is that the vena cava in its postrenal portion is not a new channel, as held by Rathke (’30), but rather that it is the transformed right posterior cardinal vein. Subsequent investigations of Zumstein (’98) on the mole and of Grosser (’01) on the bat seemed to indicate that the scheme of development in the rabbit, as described by Hochstetter, applied equally well to these species.

Lewis (’02), in repeating the work of Hochstetter on the rabbit, recognized that the two veins, one lying on the medial side of each mesonephros, are bilaterally symmetrical in early stages and that they antedate the presence of a posterior Vena cava as such. To these paired channels Lewis gave the name ‘subcardinal veins.’ Zumstein had earlier noted the presence of these veins, but, as Lewis states, did not appreciate the importance of his observations. During the course of development a connection by way -of the oaval mesentery takes place between the liver sinusoids and the right subcardinal vein. This connection has later been termed the ‘hepato—subcardinal junction.’ As a result of the formation of this junction, there is laid down the prerenal portion of the posterior Vena cava, made up of four embryonic components: the Vena hepatica communis of Hochstetter, the hepatic sinusoids, an independent vein within the cava.l mesentery, and a portion of the right subcardinal vein. Concerning the development of the DEVELOPMENT OF THE POSTERIOR VENA CAVA 271

postrenal portion of the cava in the rabbit, Lewis’s investigation adds nothing to the descriptions of Hochstetter, Zumstein, and Grosser.

The work of Huntington and McClure (’07, ’20) was based primarily on a study of the veins in the cat. Previous investigations had established rather deﬁnitely the fundamental factors involved in the formation of the anterior portion of the posterior vena cava; the knowledge concerning the more posterior or postrenal portion of the cava, however, had proved insufficient for an interpretation of the conditions found in cat, pig, human embryos, etc., and for interpretation of the atypical conditions so frequently observed in adult mammals. The outstanding contribution of the work of Huntington and McClure consists in the identiﬁcation of a pair of venous channels, heretofore unrecognized, which they named the ‘supracardinal system’ of veins. In the thoracic region the supracardinal veins contribute largely to the formation of the adult azygos veins, while in the lumbar region the fused right and left supracardinals are transformed into the adult posterior vena cava. It was demonstrated that in the cat “the right posterior cardinal vein does not in the slightest degree, a hitherto supposed, enter into the formation of the postrenal division of the posterior vena cava.” Huntington and McClure were able, furthermore, to construct a composite diagram or ontogenetic plan which includes all of the embryonic veins of the cat which make their appearance, at one time or another, during the course of development. On the basis of this plan, one is able to interpret clearly and deﬁnitely those variant conditions, so frequently found in adults, which are due to modiﬁcations of the typical course of venous development.

Subsequent work on human embryos (McClure and Butler, ’25) has shown that in man the development of the posterior vena cava is essentially the same as in the cat, and that the minor differences found represent variations in the role which the embryonic veins (posterior cardinal, subcardinal, and supracardinal) play during the course of ontogeny. For 272 ELMER G. BUTLER

details of the transformations and alterations of the embryonic veins in the cat and in man, the reader should refer to the original papers on the subject.

PRESENT INVESTIGATION

As the writer has stated above, the aim of the present investigation has been to study by the method of comparative embryology, in as comprehensive a manner as possible, the problem of the development of the posterior vena cava in a group of different mammals. The endeavor has been one not merely of cataloguing the details of development in the different forms, but rather of bringing together the knowledge gained from a study of all into a uniﬁed conception of the development of this vein in mammals. The method of comparison and correlation leads to the establishment of fundamental conclusions impossible from a study, no matter how detailed or intensive, of a single individual form; in the case of the posterior vena cava, it leads especially to the recognition of at least some of the primary, developmental factors which inﬂuence and govern the establishment of this main venous pathway.

The embryos utilized have been those of the pig, sheep, bat, rabbit, and rat. Several factors have governed the selection of these particular species, chief of which have been the availability of good embryos and the obtaining of those which exhibit differences in morphological characteristics, especially in the size of the mesonephroi. As will be shown in following pages, it is evident that the size and functional activity of the mesonephroi play an important part in governing the transformation of embryonic veins associated in the development of the vena cava. On this basis, the embryos mentioned above comprise a representative series for the purposes of the present work.

The presentation of the results of this study conveniently separates itself into two divisions: First, an account of the salient features of development in each of the animals studied; secondly, a consideration of the general conclusions DEVELOPMENT on THE POSTERIOR VENA CAVA 273

which may be drawn from such foregoing individual studies, including those on the cat and man. Although a knowledge of the details of development in the several forms is prerequisite to the drawing of generalizations, it is the latter which are of the more fundamental importance and signiﬁcance and which form the thesis of this paper.

A complete tabulation of the embryos studied during the course of this investigation will not be attempted. It may be-said, however, that, so far as possible, all available embryonic stages of the mammals mentioned have been examined. Those at critical stages have been reconstructed in wax after the method of Born. The following is a list of the reconstructed embryos.

Pig embryos reconstructed

Princeton no. 155, 5- mm. embryo Princeton no. 215, 14- mm. embryo Princeton no. 126, 6- mm. embryo‘ Princeton no. 141, 17- mm. embryo Princeton no. 161, 9- mm. embryo Princeton no. 167, 17- mm. embryo‘ Princeton no. 162, 12- mm. embryo‘ Princeton no. 195, 22- mm. embryo Princeton no. 610, 12- mm. embryo Princeton no. 1625, 31.5-mm. embryo

Bat embryos reconstructed’

Princeton no. 1661, 5- mm. embryo Princeton no. 1664, 6.5-mm. embryo Princeton no. 1662, 5.5-mm. embryo Princeton no. 857, 8- mm. embryo Princeton no. 1656, 6- mm. embryo

Sheep embryos reconstructed

Harvard no. 1106, 14- mm. embryo Harvard no. 1237, 15.8-mm. embryo Harvard no. 1108, 14.1-mm. embryo Harvard no. 2118, 17- mm. embryo

Rut embryos‘ reconstructed

Columbia no. 799, 7- mm. embryo“ Columbia no. 849, 11- mm. embryo" Columbia no. 873, 8.5-mm. embryo‘ Columbia no. 1913, 11- mm. embryo‘ Columbia no. 993, 9- mm. embryo‘ Columbia no. 796, 12- mm. embryo‘ Columbia no. 902, 10- mm. embryo‘

Rabbit embryos reconstructed Harvard no. 1237, 11-mm. embryo Harvard no. 158, 13-mm. embryo

‘Reconstructed by Dr. E. L. Shaffer.

’ These embryos were collected in 1913 for the Princeton Embryological Collec tion by Dr. F. P. Reagan. “Reconstructed by Dr. George S. Huntington. ‘Recontructed by Mr. E. M. Shearer. 274 ELMER G. BUTLER

DEVELOPMENT OF THE POSTERIOR VENA CAVA IN THE PIG

On the basis of observations made on embryos of other mammals, a satisfactory interpretation of the method of venous development in the pig has, up to the present time, been difficult. Only two investigations of importance have preceded this study of the development of the posterior vena cava in the pig, those of Davis (’10) and Sabin (’15). The work of Davis consisted principally in a careful study of the formation of the hepato-subcardinal junction and does not attempt to add to the knowledge of the development of the cava caudal to this point. The investigation of Sabin (’15) deals with the formation of both the vena cava and azygos veins. Unfortunately, the nomenclature used in the latter paper is different from that previously employed. The subcardinal veins (Lewis, ’02) become the mesial cardinal .veins, while the supracardinal veins (Huntington and McClure, ’07) are designated as a prevertebral plexus. Sabin demonstrated, however, that in the pig, as in the cat, the posterior cardinal veins disappear with the mesonephroi and play no part in the formation of the posterior vena cava.

For the purposes of the present study, careful examination has been made of closely graded stages of pig embryos between the ages of 5 mm. and 32 mm. in length. Such a study, it is believed, has made possible a clear and accurate understanding of the developmental transformations of the main venous channels. For facility of description and ease of understanding, the developmental process has been divided into eight succesive stages from the 5-mm. embryo to the adult, each stage being illustrated, by a diagram. Taken together, the eight diagrams present, as nearly as possible, an accurate representation of the ontogenetic stages leading up to the establishment of the adult venous system.

For the sake of completeness, transformations of embryonic vessels other than those associated strictly with the formation of the posterior vena cava, such as the anterior cardinal veins, the common cardinal veins (ducts of Cuvier), and the thoracic portions of the posterior cardinal and supracardinal DEVELOPMENT OF THE POSTERIOR VENA CAVA 275

veins, have been included. In this connection the writer fully appreciates and acknowledges the work of previous investigators, particularly that of Reagan (’19) on the development of the azygos veins in the pig.

THE CARDINAL VENOUS SYSTEM IN YOUNG MAMMALIAN EMBRYOS Figure 1

Embryos below 5 mm. in length exhibit an elementary plan of the venous system in which there are three pairs of bilaterally symmetrical veins—the umbilical (T/'.Umb.), the omphalomesenteric (V.Om.), and the cardinal (Pro. and Pc.). Of these, the anterior (Prc.) and the posterior cardinal (Pc.) veins are the chief drainage channels of the body proper. The posterior cardinals (P0,) at this stage are already comparatively large vessels, arising in the extreme caudal part of the embryo and extending anterior, in a position dorsal to the mesonephroi, to open into the sinus venosus by way of the common cardinal veins (D.C.). Each posterior cardinal vein (Pc.) receives segmental tributaries from the dorsal body wall, but has for its prime function the drainage of the mesonephros. Tributaries arise both on the medial and lateral surface of each mesonephros and, extending dorsal, empty at frequent intervals into the posterior cardinal vein. .

An elementary cardinal plan such as this is present in all young mammalianembryos and forms the starting-point for the series of venous modiﬁcations leading up to the adult stage.

5-MM. TO 6-MM. EMBRYOS

Figure 2

Subcawdmal veins. Early in the development. of the pig there appear two new longitudinal and bilaterally symmetrical venous channels, the subcardinal veins (Saba) and the ventral veins of the mesonephroi (_ V.v.Dear;t. and Sin.). The subcardinal veins originate as a result of the coalescence of those early tributaries of the posterior cardinal veins which

lie medial to the mesonephroi and drain the glomerular region 276 ELMER G. BUTLER of this organ. Each subcardinal vein in embryos of between 5 mm. and 6 mm. starts near the caudal end of the mesonephros and extends anterior just Ventral to a row of mesonephric arteries. During its course the subcardinal vessel (Saba) connects with the posterior cardinal vein (Pc.) by numerous subcardino-posterior cardinal anastomoses (Anast-.Subc.Pc.), which represent the persisting intermediate portions of the former medial cardinal tributaries (ﬁg. 1). On each side of the body the subcardinal Vein terminates at the head of the

mesonephros, where it opens into the posterior cardinal.

EXPLANATION OF FIGURES

A uniform scheme of representing the diiferent embryonic vessels has been followed throughout the series of diagrams; cardinal veins are black, subcardinal veins are stippled, supracardinal veins are cross-lined, etc.

The short arrows (A, B, C, etc.) in the diagrams indicate the level of the cross sections correspondingly labeled.

The long arrows (X and Y) in the diagrams indicate the relations which the permanent kidneys (metanephroi) and ureters bear to the veins.

ABBREVIATIONS

Anast.Subc.Sprc.De:I:t. (P.Ren.), right subcardino-supracardinal anastomosis

A., lumbar division of right posterior cardinal vein (V. cardinalis pos terior dextra), ﬁgure 26

Adm, adrenal vein (V. adrenalis, suprarenalis), ﬁgure 26

A.0m., omphalomesenteric artery (A. omphalomesenterica)

A.Umb., umbilical artery (A. umbilica)

Ana.9t.Il.Pc., anastomosis between posterior cardinal veins at level of iliac veins

Anast.Int.Sp'rc., interupracardinal anastomosis. Anastomosi between supracardinal veins

Anast.Int.Subc., intersubcardinal anaetomosis (anastomosis, caudal to omphalomesenteric artery, between subcardinal veins)

Anast.Subc.Pc., subcardino-posterior cardinal anastomosis. Anastomosis between subcardinal and posterior cardinal veins

Anast.Subc.Sprc., Subcardino-supracav dinal anastomosis. Anastomosis between subcardinal and supracardinal veins

(pars renalis of vena cava posterior)

A'nast.Subc.V.1:., anastomosis between the subcardinal vein and the ventral vein of the mesonephros

Amtst.V.1;.Pc., anastomosis between the ventral vein of the mesonephros and the posterior cardinal vein

Ao., aorta

Az., azygos vein (V. azygos)

B., lumbar division of right supracardinal vein (V. supracardinalis dextra), ﬁgure 26

0., lumbar division of left supracardinal vein (V. supracardinalis sinistra), ﬁgure 26

0.0., cardinal collateral vein (V. cardinalis collateralis)

Coel., coelom

D., lumbar division of left posterior cardinal vein (V. cardinalis posterior sinistra), ﬁgure 26

D.C'., common cardinal vein (duct of Cuvier)

Dea:t., dextra DEVELOPMENT OF THE POSTER-IOR VENA CAVA

E.Il.V., external iliac vein (V. iliaca externa), ﬁgure 26

Hem.A2., hemiazygos vein (V. hemiazygos)

Hep.Su.bc.Jct., hepato-subcardinal junction (junction made between hepatic sinusoids and right subcardinal vein)

I.Il.V., internal iliac vein (V. iliaca interna), ﬁgure 26

I1m0m.Sin., left innominate vein (V. anonyma sinistra)

Int.Sabc.A1mst., intersubcardinal anastomosis (anastomosis, caudal to omphalomesenteric artery, between subcardinal veins), ﬁgure 26

Jug.Ezt., external jugular vein (V. jugularis externa)

Jug.I'rI,t., internal jugular vein (V. jugularis interna)

K., permanent kidney (metanephros)

L.Imwm.V., left innominate vein (V. anonyma sinistra), ﬁgure 26

Mes.Caud.T*rt'b., caudal mesonephric tributary which opens into the supracardinal vein

Meson., mesonephros

P.0ard., pars cardinalis of vena cava posterior in rat

P.Hep., pars hepatica of vena cava posterior

P.Re2c., pars renalis of vena cava'posterior

P.Subc., pars subcardinalis of vena cava posterior

P.Sprc., pars supracardinalis of vena cava posterior

Pc., posterior cardinal vein (V._cardinalis posterior)

Pc.(Az.), posterior cardinal vein in azygos region

Pm, anterior cardinal vein (V. cardinalis anterior)

Prom, anterior vena cava (V. cava anterior)

R.Col., lateral portion of renal collar (subcardino-supracardinal anastomosis)

277

R.V., renal vein (V. renalis), ﬁgure 26

Rem, renal vein (V. renalis)

S.V., sinus venosus in ﬁgures 2 and 3; sex veins in ﬁgure 26

Scl., subclavian vein (V. subclavia)

Sim, sinistra

Spr., suprarenal vein (V. suprarenalis)

Sprc., supracardinal vein (V. supracardinalis) \

Sprc.(Az.), thoracic or azygos division of supracardinal vein

.Sprc.De:1;t.(P,Sprc.), right supraca.rdinal vein (pars supracardinalis of vena cava posterior)

Subc., subcardinal vein (V. subcardinalis)

Subc.S2'n.(Spr.), left subcardinal vein (left suprarenal vein). V. suprarenalis sinistra

Subc.Po.Anast., subcardino-posterior cardinal anastomosis (anastomosis between subcardinal and posterior cardinal veins), ﬁgure 26

Sul2c.Sprc.Anast., subcardino-supracan dinal anastomosis (anastomosis between subcardinal and supracardinal veins), ﬁgure 26

Subc.Vent., vein along ventromedial border of mesonephros in sheep embryos ‘

U32, ureter

V.H.C., vena hepatica communis

V.Il.Eav., external iliac vein (V. iliaca. externa)

I7.Il.In., internal iliac vein (V. iliaca interna)

17.1 l.1n.Com., common internal iliac vein (V. iliaca interna communis)

V.Mes.Lat., lateral mesonephric vein; vein around the lateral side of the caudal end of the mesonephros

V .0m., omphalomesenteric vein (V. omphalomesenterica)

V.l7mb., umbilical vein (V. umbilica)

V.S.I., sex vein (V. spermatica interna)

V.12., ventral vein of the mesonephros 278 ELMER G. BUTLER

Ventral veins of the mesonephroi. In a manner similar to the origin of the subcardinal vein, that is, by anastomoses of those early tributaries of the posterior cardinal vein which lie Ventral (or ventrolateral) on each mesonephros, there originates another pair of bilaterally symmetrical, longitudinal Vessels, the Ventral Veins of the mesonephroi (V.v.Deact. and Sm). Each ventral vein of the mesonephros lies on the surface of the mesonephros in a position just




Pc. Dext.

‘\ Mesonephric * % ‘V3 Tributaries

K 7’


Fig. 1 Plan of the cardinal venous system in young mammalian embryos. DEVELOPMENT OF THE POSTERIOR VENA CAVA 279

medial to the mesonephric duct. It arises along the caudal third of the mesonephros, and extends anterior, connecting at frequent intervals by lateral anastomoses (A/na,st.V.v.Pc.) with the posterior cardinal Vein (Pc.), into which it ﬁnally opens only slightly cranial to the point of opening of the

Fig. 2 Diagram of the venous ystem of'5-mm. to 6-rnm. pig embryos. Section A is from a '5-mm. pig embryo," Princeton Embryological Collection, series 155, slide 3, section 27. 280 ELMER G. BUTLER

subcardinal vein (Subcu). It is clearly evident by a study of embryos between 5 mm. and 10 mm. in length that the ventral mesonephric veins in early pig embryos are as important functionally as are the subcardinal veins. However, they are channels which are characteristic, so far as is known, only of pig cmbryos;5 they have no evolutionary signiﬁcance, and, since they disappear during the course of later development, they play no part in the formation of the adult venous system. This stage of venous development in the pig, represented by a bilaterally symmetrical plan of cardinal (Pro. and Pc.), subcardinal (Saba), and ventral mesonephric veins (VAL), is entirely comparable to the cardino-subcardinal stage previously described in the cat (Huntington and McClure, ’20) and in man (McClure and Butler, ’25). The addition in the pig of a third pair of vessels, the ventral veins of the mesonephroi, evanescent in character, is associated with the relatively large size of the mesonephroi and the consequent necessity for a more eﬂicient drainage of these organs.

6-MM. T0 7 —MM. EMBRYOS

Figure 3

H epat0—subcairdz'nal junction. In embryos between 6 mm. and 7 mm. in length there occurs the ﬁrst critical modiﬁcation of the elementary symmetrical venous plan. This modiﬁcation consists in a union, through the caval mesentery, between the hepatic sinusoids and the right subcardinal vein (Subc.Deact.) forming the hepato-subcardinal junction (H ep.Subc.J ct.). The result is the establishment of the prerenal division of the posterior vena cava, which, as in all mammals thus far investigated, is formed from the vena hepatica communis of Hochstetter, the hepatic sinusoids, an independent vein Within the caval mesentery, and a portion of the right subcardinal vein. The prerenal division of the posterior vena cava may, therefore, be conveniently described as consisting of two main embryonic subdivisions, the pars hepatica (P.Hep.), which is

“Ventral mesonephric veins are occasionally found in embryos of other mammals, but they are never as large or as functionally important as in the pig. DEVELOPMENT 013‘ THE POSTERIOR VENA CAVA 281

the portion of the Vena cava lying cranial to the hepato—subcardinal junction, and the pars subcardinalis (P. Subc., Subs. Dea:t.), the portion of the prerenal division of the Vena cava caudal to the hepato—subcardinal junction.

Intersubcwrdmal cmastomosis. Associated with the formation of the hepato-subcardinal junction (Hep.Subc.Jct.) is the establishment of a. connection between the two subcardi—

Fig. 3 Diagram of the venous system of 6-mm. to 7-mm. pig embryos. Section B is from a 6-mm. pig embryo, Princeton Embryological Collection, series 126, slide 5, section 41. 282 ELMER G. BUTLER

nal veins (Snbc.Dent. and Sin), ventral to the aorta and just caudal" to the level of the omphalomesenteric artery, called the intersubcardinal anastomosis (Anast.Int.Snbc.). In pig embryos this anastomosis early assumes large proportions and is of primary importance in diverting the blood ﬂow from the left side of the body into the prerenal portion of the posterior vena cava. As will be shown later, it enters directly into the formation of the left renal vein of the adult.

In cennection with the establishment of the hepato-subcardinal junction and the intersubcardinal anastomosis, profound alterations overtake other venous channels of the body. Blood from the caudal half. of the body may now be returned to the heart by way of three different channels, the right posterior cardinal vein (Pc.Deaot.), the left posterior cardinal vein (Pc.Sz'n.), and the prerenal division of the vena cava (P.Snbc. and P.Hep.)‘. The vena cava is by far the most direct and least impeded of the three pathways and grows rapidly in size, while the other vessels become relatively smaller.

Breaking up of posterior cardinal veins. Changes in the posterior cardinals are particularly signiﬁcant. Along the cranial half of the mesonephros each cardinal vein (Pc.Dea>t. and ;S'z'n.) remains as a continuous channel, but as such it can be traced caudad only to about the middle of the mesonephros, i.e., to about the level of the intersubcardinal anastomosis (Anast.Int.Snbc.). Oaudal to this point the cardinal vein can no longer be followed along the -mesonephros as a continuous vessel. Its place has been taken by numerous broad tributaries, representing persistent subcardino-posterior cardinal anastomoses (An»a~st.Snbc.Pc.), which now drain the caudal portions of the mesonephros i11to the subcardinal vein (Snbca). , V.

Posterior to‘ the caudal ends" of the mesonephroi continuous posterior cardinal veins still persist. Blood from the tail region of the embryoland from the hind limb still passes into this vein i-on either side -and thence into the subcardinalvein by way of subcardino-posterior cardinal anastomoses. DEVELOPMENT OF THE POSTERIOR VENA CAVA 283

12-MM. TO 14-MM EMBRYOS

Figure 4

Diversion of the main blood ﬂow into the subcardinal veins. During the course of development between 6 mm. and 12 mm. in length, the venous organization undergoes a series of gradual modiﬁcations associated principally with the growth of the mesonephroi and the constantly increasing importance of the prerenal division of the vena cava (P.Hep. and P.Siibc.). These modiﬁcations consist for the most part in a general diversion of the blood ﬂow from all parts of the body caudal to the level of the hepato-subcardinal junction (H 610. Subo.Jct.) into the right and left subcardinal veins. As a result, these two veins (Subc.Deavt. and Sin.) in their middle and posterior portions become the largest veins of the abdominal cavity, and the intersubcardinal anastomosis (Aaiast.Int.Subc.) assumes the appearance of a broad fusion between the two.

As the diagram indicates (ﬁg. 4), the drainage of the mesonephroi is now almost entirely directed into the subcardinal veins. Only the most cranial portion of each mesonephros drains by way of the persisting anterior extremities of the subcardinal (Siibc.), ventral mesonephric (V.o.), and posterior cardinal (Pc.) veins into the common cardinal vein (D.C.). The remainder of each mesonephros is drained by large dorsal and ventral tributaries which arch dorsal and ventral around the surface of the mesonephros and empty into the subcardinal vein, principally in the region of the intersubcardinal anastomosis. The broad dorsal mesonephric tributaries _(A’l’b(1»8t.Sub0.PC.)‘ of the subcardinal are to be considered as identical with the early subcardino-posterior cardinal anastomoses, which, with the growth of the mesonephroi, have undergone a great increase in size. The ventral mesonephric tributaries (Aiiast.Siibc.V.v.) of the subcardinal arise as a result of anastomoses (established at about 8 mm. or 9 mm. in length) between the ventral mesonephric vein and the subcardinal vein.

THE AMERICAN JOURNAL or ANATOMY, von. 39, no. 2 284 ELMER G. BUTLER '

Suprareatal veins. On the right side of the body that part

of the subcardinal vein (Subc.Deoct., Spr.) originally extending between the hepato-subcardinal junction (H ep.Subc.J ct.) and the posterior cardinal vein (Pc.Deact.) is no longer a continuous vessel. The portion of this vein (Subc.Deact., Spr.) which still connects with the pars subcardinalis of the vena cava at the hepato-subcardinal junction has become at this stage intimately associated with the developing right suprarenal gland and is the chief drainage channel of this organ. It eventually becomes the right suprarenal vein of the adult. A similar modiﬁcation has overtaken the left subcardinal vein (Subc.Sm.,Spr.) anterior to the intersubcardinal anastomosis, so that from this stage on it may be considered as the left suprarenal vein.

Oblitcmtion of the caudal portion of the posterior cardinal vein. The condition of the venous channels at the caudal end of each mesonephros in 12-mm. to 14-mm. embryos is particularly signiﬁcant for the reason that positive evidence is presented that at this stage the posterior cardinal veins in this region are being obliterated as continuous vessels, and as such, therefore, can play no further part in venous development. Up to about 12 mm. in length, the drainage of the hind-limb buds and of the caudal region of the embryo remains practically the same as in embryos of 6 mm. and 7 mm. (ﬁg. 3), namely, blood passes through the short portion of the cardinal vein which persists at the caudal end of the mesonephros, thence through subcardino-posterior cardinal anastomoses and into the subcardinal vessels. At about the age of 12 mm., however, each mesonephros has attained such relatively great proportions and extends so far caudal in the body cavity (actually to the level of the umbilical arteries) that, as a result, the plan of venous drainage in the posterior portion of the body is altered to a very marked degree. Blood from the hind-limb buds and caudal end of the body now enters directly the venous plexus at the caudal end of each mesonephros and passes for some distance craniad through a vessel (V.Mes.Lat.) which lies on the lateral surface of the DEVELOPMENT OF THE POSTERIOR VENA (JAVA 285

Sci.



P. Hep. Subc. Dex1’..($pr.)

Hep. Subc. Jet.

Anast . Su bg:.V.v.

Anast. Su be. Pc.

V. Mes.Lni'..Dext.

Fig. 4 Diagram of the venous system of 12mm. to 14-mm. pig embryos. Section 0 is from a 14-mm. pig embryo, Princeton Embryological Collection, series 215, slide 16, section 21. 286 ELMER G. BUTLER

mesonephros. This lateral vessel, extending craniad for a variable distance, usually to a level slightly posterior to the intersubcardinal anastomosis (Anast.Int.Subc.), then passes round the dorsal surface of the mesonephros (Avnastﬂubc. Po.) and joins the subcardinal vein (Saba). Such an arrangement of Vessels is of great signiﬁcance; it demonstrates that at this stage each posterior cardinal vein in its caudal portion has lost its former identity as a continuous Vessel and has been superseded functionally by a more lateral mesonephric channel.

Each newly formed lateral mesonephric vein (V.Mes.Lat.) is a vessel which arises from the venous plexus on the lateral surface of the mesonephros to fulﬁll the office of a temporary drainage channel for the developing hind limb and the caudal end of the body. The fact that it is not present in many 12—mm. embryos,“ which still retain the earlier plan, indicates that the 12-mm. stage represents the crucial period for the disappearance of the posterior cardinal veins in this region. It is clear, moreover, that those embryos of 12 mm. in which the lateral vein (V.Me.9.Lat.) is present are not merely individuals presenting an atypical condition of the mesonephric plexus, since this vein is invariably found in older embryos up to 17 mm. in length.7 At this time the lateral veins themselves are superseded functionally by a new pair of channels —the supracardinal system of veins.

17—MM. TO 19-MM. EMBRYOS

Figure 5

Supmcardmal veins. In embryos of 15 mm. to 16 mm. there appears a new pair of symmetrical, longitudinal venous channels—the supracardinal system of veins (Sprc.Decct. and Sin.)

‘One-half of the sixteen 12-mm. pig embryos in the Princeton Embryological Collection which are sectioned transversely possess the lateral vessel; the other half exhibit the same condition at the caudal end of the mesonephros as that found in younger embryos.

7 The lateral mesonephric vein here described has been previously observed by Lewis (’02), who brieﬂy refers to it as follows: “In pig embryos of 12.0 mm. the main cardinal vessel passes to the outer side of the caudal end of the Wolﬂian body uninﬂuenced by the renal anlage.” Because of its location and its apparent manner of origin, the present writer believes that this lateral vein is not the original cardinal channel found in younger embryos. DEVELOPMENT OF THE POSTERIOR VENA CAVA 287

which are located on either side of the body, both in the thoracic and lumbar regions, in a position dorsolateral to the aorta. Since they appear in the pig, as they do also in the case of cat and of man, in these two separate regions of the body, the

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Fig. 5 Diagram of the venous system of 17-mm. to 19-mm. pig embryos. Section D is from a 17-mm. pig embryo, Princeton Embryological Collection, series 167, slide 28, section 19. 288 ELMER G. BUTLER

supracardinal veins in the lumbar region cannot be regarded as merely a synonym for the dorsal limb of the periureteric venous rings in the rabbit ﬁrst described by Hochstetter, but rather they comprise a morphologically uniform system of longitudinal channels which develop parallel to the line of the old posterior cardinal veins and ultimately contribute to the establishment of the azygos veins and a portion of the postrenal division of the posterior vena cava (pars supracardinalis). For the sake of clearness, in the accompanying diagrams the supracardinal veins have been placed farther apart than they are actually located in the embryo where they lie relatively close to the sympathetic trunks on each side and frequently anastomose with each other dorsal to the aorta, particularly in the later stages.

Although at the 15—mm. to 16-mm. stage the supracardinal veins are small vessels often followed with difficulty, they increase rapidly in size, and in 17-mm. to 19—mm. embryos (ﬁg. 5) are present as symmetrical vessels of considerable size and importance in both the thoracic and the lumbar regions of the body. In the lumbar region the supracardinal veins (Sprc.Dext. and Sin.) arise at the level of the hind—limb buds and may be traced craniad to a point about opposite the middle of the intersubcardinal anastomosis (Ana,st.Im‘.Subc.). The thoracic supracardinals (Spra, As), both essentially of the same caliber, join the posterior cardinal veins (Pc.) slightly cranial to the point where the subcardinal (Saba) and ventral mesonephric veins (I/Xv.) open into the cardinal. From here they may be traced posterior to a point slightly cranial to the level of the intersubcardinal anastomosis. It is not unusual, especially in the later stages, to ﬁnd that the lumbar and thoracic supracardinals are continuous vessels throughout their entire length. This offers evidence for the potential continuity of these vessels in the pig.

Subcardmo-supracardinal cma,st0m0se.s. Associated with the formation of the supracardinal veins in the lumbar region is the establishment of an important Vessel, at ﬁrst plexiform in character, by means of which each lumbar supracardinal DEVELOPMENT on THE‘ POSTERIOR VENA CAVA 289

vein (Sprc.Demt. and Sin.) becomes connected with the laterocaudal border of the intersubcardinal anastomosis (Anast.Int.Snbc.). This vessel, the subcardino-supracardinal anastomosis (Anast.Snbc.Sprc.Dent. and Stn.), passes in a ventrocraniad direction. in the region between the head of the migrating kidney (metanephros) and the aorta. It is entirely comparable to the lateral side of the renal collar in the cat, in which at this stage there is a complete venous ring encircling the aorta (Huntington and McClure, ’20). In pig embryos the fusion of the supracardinal veins dorsal to the aorta in this region has never been observed, and thus the dorsal component of a complete circumaortic venous ring is lacking.

Embryontc components of the adult posterior vena cava. The appearance of the supracardinal veins and the subcardino-supracardinal anastomoses marks the establishment in the embryo of the postrenal division of the vena cava, which is made up from two sources, the right supracardinal vein (Sprc.Deaot.) and the right subcardino-supracardinal anastomosis (Anast.Sn~bc.Sprc.Deact.). As in the cat and in man, the former will be called the pars supracardinalis (P.Spr(:.), the latter will be called the pars renalis (P.Ren.). As noted above, the prerenal division of the vena cava has already been established as a result of the formation of the hepato-subca.rdinal junction. Therefore, we have now laid down throughout its entire length the posterior vena cava, which in its entirety consists of the following four subdivisions: pars hepatica (P.Hep., vena hepatica communis, liver sinusoids, and an independent‘ vein within the caval mesentery); pars subcardinalis (P. Snbc. portion of the right subcardinal vein); pars renalis (P.Ren., right subcardino-supracardinal

anastomosis); pars supracardinalis (P.Sprc., right lumbar supracardinal vein).

With the advent of the lumbar supracardinal veins (Sprc. Dent. and Sin), which drain the caudal end of the body and the hind-limb buds, the lateral veins round the caudal third of each mesonephros (V.Mes.Lat.Dewt. and Sin), which 290 ELMER G. BUTLER

arose at the 12—mm. stage, become vessels of little importance, and frequently in embryos of 17 mm. to 18 mm. these veins have lost their caudal connections with the limb tributaries and serve merely as veins draining the posterior ends of the mesonephroi.

In passing, it is interesting to note the tardiness in the pig of the formation of the anastomosis between the veins of either side of the body in the region of the iliac Veins. In human embryos this iliac anastomosis between the posterior cardinal veins is established before the appearance of the supracardinal Veins, and in the cat its formation is about coincident with their appearance. A consideration of attendant circumstances indicates that the absence of such a union in the pig at an earlier stage of development is associated chieﬂy with the great size and importance of each subcardinal vein (Saba) and with the drainage of the hind limbs into the particularly well-developed mesonephric subcardinal tributaries.

22-MM. TO 24—MM. EMBRYOS

Figure 6

Enlargement of postremtl division of vena ccwa. The most noticeable and signiﬁcant modiﬁcation in embryos of from 22 mm. to 24 mm. is the establishment of an asymmetrical venous plan in the lumbar region. The right supracardinal vein (Sprc.Deact., P.Sprc.) and the right subcardino-supracardinal anastomosis (Anast.Szob0.S19rc.Dea:t., P.Ren.)—in other Words, the pars supracardinalis and pars renalis of the posterior vena cava——increase greatly in size, while the corresponding vessels on the left side (the left supracardinal vein and the left subcardino-supracardinal anastomosis) become relatively smaller. Associated with this enlargement of the main caval channel is the formation of the iliac anastomosis (Amzstll. Pa), uniting the caudal ends of the right and left supracardinals so that an increasingly greater amount of blood from the left hind—limb bud is directed into the vena cava. This anastomosing vessel (Am1ust.Il.Pc.) eventually enters directly into the formation of the left common iliac vein of the adult. DEVELOPMENT or THE POSTERIOR VENA CAVA 291

Frequent intersupracardinal anastomoses (Anwst.Int.Sprc.) dorsal to the aorta are present in both the lumbar and thoracic regions of the body. As a rule, they are more numerous between the thoracic supracardinal veins.







P¢.(A:)$in. Anas’(..I’n1’.. Spa-c.

V.v. Sin.

sprc. Sin. subc. Sin.

Subs. Dnx7..(Spr.) s..L._sa..(s,.-;

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Fig. 6 Diagram of the venous system of 22-mm. to 24-mm. pig embryos. Section E is from a 23-mm. pig embryo, Princeton Embryological Collection, series 67, slide 49, section 13. 292 ELMER G. BUTLER

The cranial pole of each mesonephros still drains into the common cardinal vein (D.C.) through the persistent proximal ends of the posterior cardinal (Pc., 112.), the subcardinal (Saba), and the ventral vein of the mesonephros (V.v.). The remainder of each mesonephros drains into the subcardinal vein, chieﬂy at the level of the intersubcardinal anastomosis.




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Fig. 7 Diagram of the venous system of 30—mm. to 35-mm. pig embryos. DEVELOPMENT OF THE POSTERIOR VENA CAVA 293 30—MM. T0 35—MM. EMBRYOS Figure 7

FINAL TRANSFORMATIONS LEADING UP TO THE ADULT CONDITION Figure 8

In embryos of from 30 to 35 mm. in length (ﬁg. 7) are foreshadowed in all essentials the ultimate plan of organization







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8

Fig. 8 Diagram of the venous system of an adult ﬁig 294 ELMER G. BUTLER

of the adult Vena cava and its tributaries (ﬁg. 8). The drainage of the cranial pole of each mesonephros into the common cardinal vein (D.C.) has been lost. The mesonephroi, in both their anterior and their middle regions, now drain through the dorsal and Ventral mesonephric tributaries into the subcar— dinal Veins chieﬂy at the level of the inter-subcardinal anastomosis. Transformation of the venous system of an embryo of this age into that of an adult consists principally in the elimination of these inesonephric tributaries.

Sea: veins. Both right and left sex Veins (V.S.I.Deact. and Sin.) in the adult pig (ﬁg. 8) join the Vena cava not far cranial from the junction of the common iliac veins; the vein from the left gonad passes dorsal to the aorta.8 This dissimilarity in the adult arrangement of sex veins from that in the adult cat and in man suggests that the manner of origin may also be different, and such, indeed, appears to be the case. So far as can be determined, the subcardinal veins contribute not at all to ‘the formation of the sex Veins in the pig as they do both in the cat and in man.

With relation to the development of sex Veins, the venous drainage from the caudal ends of the mesonephroi in embryos of from 30 mm. to 35 mm. (ﬁg. 7) is of particular signiﬁcance. In a 32—mm. embryo, for example, the writer ﬁnds that the right mesonephros near its caudal end has established a connection with the pars supracardinalis of the Vena cava by way of a short Vessel (Mes.Ca.ud.Tm'b.,V.S.I.Deact.) which passes ventral to the ureter. By a similar caudal mes0nephric vein (Mes.Camd.Tm'b.,V.S.I.Sm.) the left mesonephros opens into the persisting caudal portion of the left supracardinal Vein (Sprc.Sm.) and thence into the Vena cava by Way of intersupracardinal anastomoses (A'nast.I'n~t.Sprc.) dorsal to the aorta. Thus the caudal extremity of each mesonephros drains directly into the posterior Vena cava at a point only slightly cranial to the common iliac veins. At this stage

‘It is interesting to note that the connections of right and left sex veins with the posterior Vena cava are identical in the pig and in the axis deer (McClure, ’06). DEVELOPMENT OF THE POSTERIOR VENA CAVA 295

of 32 mm. the gonads are still rather far anterior in the abdominal cavity, being located on the mesonephroi not far caudal to the intersubcardinal anastomosis into which they drain by way of mesonephric and subcardinal veins. As the gonads migrate posteriorly during the course of later embryonic development, it seems highly probable that eventually they come to drain into the posterior vena cava through the caudal mesonephric veins and that these veins eventually become the adult sex veins (V.S.I.Dext. and Sim). In order to establish with absolute certainty this manner of origin of sex Veins in the pig, it would be necessary to examine much older embryos than any studied during the course of this investigation. However, with the evidence at hand the above interpretation would appear to be the correct one.

Although the precise method of the formation of sex veins in the pig differs from that in the cat and in man, it is important to note that the fundamental pri.nciple involved in their origin is essentially the same. In the case of human embryos, for example, the gonad on either side drains into a mesonephric vein which opens into the subcardinal vein (McClure and Butler, ’25). On the basis of this embryonic plan of drainage, we conclude that each sex Vein in adult man is made up of two embryonic components, one representing an embryonic mesonephric vein, the other representing a portion of the embryonic subcardinal vein. The essential point, in other words, is that each sex vein of the adult represents a small persisting unit of the embryonic mesonephric drainage system. The pig, in contrast with man, exhibits merely another method of the transformation of a portion of this embryonic mesonephric venous system into the adult sex vein. In the case of the pig, it is the caudal mesonephric vein (Mes.Caud.Tm'b.), opening into the supracardinal on either side, which is utilized and which enters directly into the formation of the adult sex vein.

Renal veins. When each permanent kidney (K) has migrated craniad to a point Where the hilum lies about opposite the subcardino-supracardinal anastomosis (Amzstﬂubc. 296 ELMER G. BUTLER

Sprc.) it establishes a venous connection with this anastomosis. On the right side of the body this connecting vein (Ren.Dea0t.) becomes the right renal vein, which in the adult opens into the pars renalis (P.Ren.,Anast.S'ubc.Sprc.Dext.) of the posterior vena cava. The left renal vein (Ren.Sm.) arises in a similar manner; in addition, however, to the vein which connects the kidney with the left subcardino—supracar~ dinal anastomosis, the left renal vein of the adult is made up of two other embryonic components, namely, the cranial portion of the subcardino~supracardina.1 anastomosis (Amzst. Subc.;S'prc.Sm.) and the intersubcardinal anastomosis (A4/east. Pm5.Subc.). Thus, the left renal vein in the adult opens into the pars subcardinalis (P.Subc.) of the vena cava slightly cranial to the opening of the right renal Vein.

Suprwrenal veins. The origin of the suprarenal Veins of each side (Spr.Dext. and Sin.) from the anterior portions of the subcardinal veins has already been discussed. Suprarenal veins in the pig differ in no essential feature, either in their manner of development or in their adult condition, from those in the cat and in man.

THE VENOUS SYSTEM OF SHEEP EMBRYOS

A survey of the investigations dealing with the develop ment of the posterior vena eava indicates that, save for the rather fragmentary observations of Hochstetter (’93), no deﬁnite study of sheep embryos has been made since the early work of Rathke (’30, ’38). During the course of the present investigation, therefore, the writer has examined the venous system in sheep embryos in practically all stages of development between the ages 8 mm. and 24. mm. in length. The most outstanding feature revealed by this study is a remarkable individual variation among several embryos of very nearly the same age. This variation is so striking and illustrates so clearly the manner in which differences may occur within a single species in the relative role of embryonic channels that it has been made the central subject of the present discussion. The variations found by the writer occur DEVELOPMENT on THE POSTERIOR VENA CAVA 297

in embryos between the ages of 14 mm. and 17 mm. in length and are essentially differences in the relative development and utilization of the posterior cardinal, subcardinal, and other closely allied veins. These differences give rise to most unusual conditions, some of which are strikingly remindful of those found in embryos of the marsupial, Didelphys (McClure, ’06). Whether variation is the rule in the sheep, as in Didelphys, or Whether the writer is dealing here with exceptional, aberrant conditions must remain an open question until a larger number of sheep embryos betvveen the ages of 14 mm. and 17 mm. can be examined. In any event, the dissimilarities in the venous system in the lumbar region of the four embryos described in following pages are of greatest interest and signiﬁcance from the comparative standpoint.

Except for the variations occurring during this rather short period of development, the embryology of the posterior vena cava in the sheep corresponds closely with that in the pig. The prerenal division of the cava, formed as a result of the establishment of the hepato-subcardinal junction, is made up of the same embryonic components—a pars hepatica and a pars subcardinalis. Supracardinal veins develop in the sheep at about the same time and to the same extent as they do in the pig; the postrenal division of the vena cava, therefore, is made up of a pars supracardinalis from the right supracardinal vein and a pars renalis from the right subcardino—supracardinal anastomosis. In all details, other than the individual variations in the sheep, it may be said that the development of the veins are more closely similar in the pig and the sheep than in any other two mammals studied. This similarity is probably due primarily to the correspondence in size and functional activity of the mesonephroi, since, as will be pointed out more speciﬁcally later, the development of the posterior vena cava is closely linked with mesonephric activity.

In preceding pages it has already been shown that, in the pig, after the breaking up of the posterior cardinal veins 298 ELMER G. BUTLER

along the caudal ends of the mesonephroi, the blood from the hind-limb buds drains directly into the mesonephric circulation, passing through the lateral mesonephric Vein round the lateral side of each mesonephros. Similar lateral Veins are found in the sheep, but, as the following embryos demonstrate, the temporary channels through the mesonephric circulation in sheep embryos are more often medial to the mesonephros rather than lateral. In one case it will be found that the subcardinal Vein itself has been utilized as the main drainage channel for the hind«limb bud and caudal end of the body. It is the variation in the utilization of lateral and medial mesonephric vessels during the critical stage after the breaking up of the posterior cardinal veins and before the appearance of supracardinal channels which has given rise to the unusual conditions in the sheep embryos described in following pages.

Since the earlier and later stages in the formation of the caval Vein are virtually identical in sheep and in pig embryos, ﬁgures of sheep embryos younger than 14 mm. or older than 17 mm. are not presented. The early transformations of the elementary cardino-subcardinal plan, such as the establishment of the hepato~subcardinal”junction, the intersubcardinal anastomosis, and the breaking up of the cardinal veins in their middle thirds, follow the same course in the sheep as in the pig; and the later changes, associated principally with the growth of the right supracardinal Vein and the right subcardino—supracardinal anastomosis, are the same in each. We shall pass directly, therefore, to a consideration of four par ticular sheep embryos of 14 mm., 14.1 mm., 15.8 mm., and 17 mm.

14-MM. SHEEP EMBR-YO HARVARD EMBRYOLOGICAL COLLECTION, NO. 1106

Figure 9 The most striking feature of the venous system of this

embryo is the presence about each umbilical artery of a complete circumumbilical Venous ring, the Ventral half of DEVELOPMENT on THE POSTERIOR VENA CAVA 299

which is much larger than the dorsal. From the circumumbilical ring on each side two veins pass craniad to the intersubcardinal anastomosis. The larger of these veins (Subc.Vent.D'e:ct. and Sin.) passes directly from the Ventral half of the Venous ring along the ventromedial border of the mesonephros, then bends sharply dorsal, crosses the medial



$ul:c.Dext. (F? Subc.) -_'l

Anast. Sul:c.Pc. ‘ it

3ubc.Vent Dext. __ i

Fig. 9 Diagram of the venous system in the lumbar region of a 14-mm. sheep embryo, Harvard Embryological Collection, series 1106. Section F is from section 674 of this series.

surface of the mesonephros, and empties into the intersubcardinal anastomosis (An-as$.Int.8ubc.). (The sharp dorsal bend of each Ventromedial vein could not be shown in the diagram of ﬁg. 9.) A much smaller Vein (V.Mes.La,t.Dext. and Sin.) extends from each circumumbilical ring round the lateral side of the mesonephros and merges with the Venous plexus dorsal to the mesonephros which empties into the

THE AMERICAN JOURNAL OF ANATOMY, VOL. 39, NO. 2 300 ELMER G. BUTLER

intersubcardinal anastomosis. This vein is identical in position and in function with the vein similarly located in pig embryos of from 12 mm. to 17 mm. (V.Mes.Lait., ﬁgs. 4 and 5). Because of the greater size of the ventral component of each circumumbilical venous ring, it is evident that most of the blood from the hind—limb buds and the caudal region of the body passes through this channel and thence to the prerenal division of the vena cava by Way of the ventromedial vein (Subc.Vemf.) along the mesonephros. This latter, although it is not in typical subcardinal position, may well be considered a part of the ‘subcardinal complex.’ It is a vessel which has arisen from the venous plexus along the medial side of each mesonephros and which, on each side of the body, replaces the subcardinal vein caudal to the intersubcardinal anastomosis; in reality, it is the subcardinal vein, transposed to a slightly different position and performing a somewhat different function.

Circumumbilical venous rings are not of infrequent occurrence in vertebrate embryos. They have been reported in embryos of reptiles and birds, and, among mammals, in embryos of the marsupials, the rabbit, the cat, and man. The presence of circumumbilical venous rings in embryos of placental mammals is of considerable morphological interest and signiﬁcance, since their ventral components (C.C.Demt. and sm.) represent the caudal continuation of the cardinal collateral veins, which, although evanescent in placentals, are highly developed in marsupials, where they enter into the formation of the posterior vena cava (McClure, ’O6). In embryos of placental mammals it is, as a rule, the dorsal posterior cardinal component of each circumumbilical venous ring which is the larger and more important. It is unusual in placentals for the ventral components of the venous rings to attain the size or the functional importance which they possess in this particular embryo. The condition of the circumumbilical rings, and, indeed, the entire venous arrangement in the lumbar region of this 14-mm. sheep, is strikingly remindful of the venous system in embryos of Didelphys. DEVELOPMENT or THE POSTERIOR VENA CAVA 301

14.1-MM. SHEEP EMBRYO

HARVARD EMBRYOLOGICAL COLLECTION, N0. 1108 . Figure 10

Although this embryo is practically the same age, according to measurement, as the one described above, there are three striking differences to be noted in its venous system: First, the Venous plan in the lumbar region is asymmetrical. Secondly, although circumumbilical Venous rings are present, it is the dorsal component of each ring which is the larger. Thirdly, small capillary supracardinal veins are present on

each side of the body.


Ana.Sl..Subc.5prc. Sim, Subc. Si n.

Fig. 10 Diagram of the venous system in the lumbar region of a 14.1-mm. sheep embryo, Harvard Embryologica] Collection, series 1108. Section G is from section 672 of this series. Diagram 10a represents a lateral view of the right side, to show the relations of the subcardinal vein, the supracardinal vein, and the kidney; mesonephric tributaries are omitted. 302 ELMER G. BUTLER

On the right side of the embryo, blood from the circumumbilical Venous ring passes craniad to the prerenal division of the vena cava principally through the right subcardinal vein (Subc.De:ct.). The right subcardinal vein, located in the typical subcardinal position, performs in this embryo exactly the same function as the Ventromedial vein (Subc.Vent.Dext.) extending along the mesonephros in the 14—mm. embryo described above (fig. 9). Such a utilization of the subcardinal Vein as the chief drainage channel for the right hindlimb bud and the caudal region of the body is very interesting. It is a condition infrequently met with and one which at once suggests the possibility of an atypical persistence of the right subcardinal vein (Su,bc.Deoot.) as the postrenal component of the posterior vena cava in an adult placental mammal.

On the left side of the body blood passes craniad from the circumumbilical venous ring through the left posterior cardinal Vein (Pc.Sm.). This makes an acute bend round the dorsal surface of the left umbilical artery, then extends along the dorsal surface of the mesonephros, and opens into the intersubcardinal anastomosis by way of a large subcardino— posterior cardinal anastomosis (Anast.Subc.Pc.) The left posterior cardinal vein, therefore, is of the same functional signiﬁcance as the right subcardinal vein.

Right and left lumbar supracardinal veins (Sprc.Dext. and Sin), located dorsolateral to the aorta, are small capillary vessels which have arisen apparently through a series of connections between the segmental Veins on each side. The right supracardinal vein (Spr0.De0ct.) can be traced as a continuous capillary channel from the circumumbilical venous ring to about the level of the intersubcardinal anastomosis. The left lumbar supracardinal vein (Sprc.S'm.), although it can be identiﬁed both in the region of the intersubcardinal anastomosis and also caudally just anterior to the circumumbilical venous ring, either is not an entirely continuous channel throughout the lumbar region, as represented in the diagram (ﬁg. 10), or else, being devoid of blood and shrunken, DEVELOPMENT or THE POSTERIOR VENA CAVA 303

it cannot be followed as such. Each supracardinal Vein connects with the intersubcardinal anastomosis (A~nast.Int.Subc.) by Way of a small subcardino—supracardina1 anastomosis (Anast.Subc.Sprc.De:1;t. and Sin), which passes in a dorso— Ventral direction between the head of the kidney and the aorta. The location of the right subcardino-supracardinal

\
'5

Pa. Sin.


Sprhocxt. 6‘ Sin. 9:. Dext.

I I c. c. Dext. 5ubc.Ven’t.. Dext.




Fig. 11 Diagram of the venous system in the lumbar region of a 15.8~mm.

sheep embryo, Harvard Embryologieal Collection, series 1237. Section E is from section 776 of this series.

anastomosis (Anast.Subc.Sprc.Deact.) and the relations of the right subcardinal (Subc.Dea7t.) and supracardinal (Sprc. Deact.) Veins to each other and to the kidney (K) are most clearly shown in ﬁgure 10 a. As in the pig, in the cat, and in man, the right supracardinal vein and the right subcardinosupracardinal anastomosis eventually make up the postrenal division of the posterior vena cava in the adult sheep. 304 ELMER G. BUTLER

15.8-MM. SHEEP EMBRYO

HARVARD EMBRYOLOGICAL COLLECTION, NO. 1237

Figure 11

This embryo exhibits two Venous modiﬁcations which are particularly noteworthy: First, a general asymmetry in the lumbar region, but an asymmetry different from that in preceding embryo; secondly, the presence on the right side of the body of a well-developed cardinal collateral vein (C'.C.Dewt.). The embryo is further characterized by the presence of the iliac anastomosis of the posterior cardinal veins (Amzst.Il.Pc.), not found in the younger embryos described above.

About the right umbilical artery is a complete circumumbilical Venous ring. From this ring blood passes craniad to the. intersubcardinal anastomosis through two veins. One of these (Subc.Vent.Dea:t.) extends from the dorsal component of the venous ring along the ventromedial border of the mesonephros to a point somewhat caudal to the intersubcardinal anastomosis, where it bends sharply dorsal and empties into the right subcardinal vein (Subc.Dext.). This ventromedial vein along the mesonephros is identical, both in location and in function, with the Vein similarly situated in the 14-mm. sheep embryo (Subc.Vemt.Dea:t., ﬁg. 4). Another vein (C'.C.Demt.), extending directly from the Ventral half of the right circumumbilical venous ring, occupies a position medial to the right ureter and close against the ventrolateral surface of the aorta. This vein appears to be homologous with the cardinal collateral Vein so prominent in the embryos of marsupials (McClure, ’06). In this sheep embryo the right cardinal collateral Vein (C'.C.Dewt.) passes craniad from the umbilical Venous ring nearly to the intersubcardinal anastomosis and then unites with the Ventromedial vein along the mesonephros (Subc.Vent.Dea:t.). Together they form the right subcardinal Vein (Subc.Deact.), which opens into the intersubcardinal anastomosis (A%ast.I%t.Subc.). DEVELOPMENT OF THE POSTERIOR VENA CAVA 305

A left circumumbilical venous ring is lacking. Blood passes from the iliac anastomosis (Ana,st.Il.P0.) round the dorsal side of the left umbilical artery to the caudal pole of the left mesonephros. From this point two veins lead craniad. One is the ventromedial vein along the mesonephros (Subs. Vent.S'in.), ‘similar in location to the corresponding vein along the right mesonephros. (Subc.Ve%t.Dea:t.) ; the other is the left lateral Inesonephric vein (V.Mes.Lat.Sm.), which, after passing round the lateral surface of the caudal end of the mesonephros, bends mediad into the old posterior cardinal line and merges with the venous plexus dorsal to the mesonephros.

Right and left lumbar supracardinal vei.ns (Spr0.Dext. and Sm.) are irregular, capillary channels. From the level of the intersubcardinal anastomosis (Anast.Int.Subc.), With which they connect by way of small plexiform subcardinosupracardinal anastomosis (Anast.Subc.Sprc.Deaot. and Sim), the supracardinal veins can be traced to about the level of the caudal end of the kidney (metanephros). Into -each supracardinal vein empty small tributaries from the. dorsal body Wall. Neither supracardinal plays any part in the drainage of the hind-limb buds.

The presence of a cardinal collateral vein (C.C.Dcact.) in this sheep embryo deserves particular consideration. Cardinal collateral veins are regularly found in embryos of marsupials, Where they enter into the formation of the posterior vena cava (McClure, ’06). Among placental mammals they have heretofore been noted in cat and in human embryos. It is seldom, however, that the cardinal collateral veins in placentals are as large or as functionally important as in the marsupials, or as is the right cardinal collateral vein (C.C.Dcact.) in this 15.8—mm. sheep embryo. The cardinal collateral vein is characteristically more medial and is closer to the aorta than is the subcardinal vein. Considering its location, there can be little doubt, therefore, of the homology between the cardinal collateral in this sheep embryo and the cardinal collaterals found in marsupials. Cardinal collateral veins are probably characteristic of the entire mammalian 306 ELMER G. BUTLER

group, but it is in marsupials that they are most highly developed.

The subcardmal complex. The presence among the foregoing sheep embryos (ﬁgs. 9, 10, and 11) of three veins, the subcardinal (Saba), the cardinal collateral (C.C.), and the ventromedial vein along the mesonephros (Subc.Vent.), all situated in the same general region and similar in function, suggests the possibility of a genetic relationship of these vessels. Shall we regard each as a vein having a distinct individuality, or are they all to be considered as closely related genetically and as members of one general venous pathway“! The latter is the simpler interpretation and, to the writer, appears to be the correct one. Concerning the subcardinal vein, Lewis (’02) states that it arises by the longitudinal anastomosis of the small tributaries of the posterior cardinal vein that lie medial to the mesonephros. McClure (’06) believes that the cardinal. collateral vein is formed through a longitudinal anastomosis between the cross

' connections of the posterior cardinal and the subcardinal

veins. From the writer’s observations, it seems evident that the ventromedial vein on the mesonephros comes from a longitudinal coalescence between the tributaries of the posterior cardinal vein which extend across the medial and the ventral surfaces of the mesonephros. All these three veins, therefore, arise by transformations in -slightly different regions of the same set of preexisting smaller vessels, tributaries of the posterior cardinal vein. The subcardinal, the cardinal c_ol1ateral, and the ventromedial vein along the mesonephros are merely three members of one general venous pathway; together they constitute what may be termed the ‘subcardinal complex’ of veins.

17-MM. SHEEP EMBRYO HARVARD EMBRYOLOGICAL COLLECTION, NO. 2118 Figure 12

The Venous plan in the lumbar region of this embryo is bilaterally symmetrical and is much simpler than that in any DEVELOPMENT on THE POSTERIOR VENA (JAVA 307

of the three_sheep embryos described above. On each side blood passes through two channels from the caudal end of the body to the intersubcardinal anastomosis. One is the lumbar posterior cardinal vein (Pa), passing along the dorsal surface of the mesonephros and opening into the intersubcardinal anastomosis by Way of a large subcardino— posterior cardinal anastomosis (Ana,st.Subc.Pc.). The other is the lumbar supracardinal channel (Spra), extending along the dorsolateral side of the aorta and connecting with the intersubcardinal anastomosis by a rather plexiform subcardino-supracardinal anastomosis (Anast.Subc.Sprc.). (The plexiform character of both the right and the left subcardino— supracardinal anastomoses is not represented in the diagram of ﬁg. 12.) The lumbar posterior cardinal and supracardinal veins, with their respective anastomoses with the intersubcardinal anastomosis, form on each side of the body a large and complete periureteric venous ring.

In this embryo there is no iliac anastomosis of the posterior cardinal veins such as that observed in the 15.8—mm. embryo (A/n»ast.Il.Pc., ﬁg. 11). It is possible that in the 15.8—1nm. embryo We have a precocious formation of this anastomosis in association with the presence of the right cardinal collateral vein. In an 18—mm. sheep embryo of the Harvard Collection (no. 1238) there is an iliac anastomosis, and, judging from the time of its appearance in pig embryos, we may suppose that the 18-mm. stage is probably the typical time for its appearance in the sheep. It is possible, moreover, that such details as this are highly variable in the sheep.

Transformation of the venous system in the lumbar region of a 17-min. embryo into that of the adult sheep is the result of relatively few changes. After the establishment of the iliac anastomosis of the posterior cardinal veins, all of the blood from the hind-limb buds and the caudal end of the body is gradually diverted into the right supracardinal vein (Sprc. Dext.). With the enlargement of this vein and the right subcardino-supracardinal anastomosis (Anast.Sulbc.Sprc. Deact.) the remaining lumbar trunks, i.e., the right posterior 308 ELMER G. BUTLER

cardinal (Pc.Dext.) and the left posterior cardinal (Pc.Sin.) Veins and the left supracardinal vein (Sprc.Sm.), gradually become smaller and ﬁnally, in the later stages of development, disappear. The right lumbar supracardinal vein and the right subcardino-supraoardinal anastomosis form, respect




Mesoneplu-ic






Tributaries A”35t- 5“b°-PC’ U Anast.In‘l..Su|:c. _ ‘ ‘fa Anast. Subcpc.

M  SAnast.:.ul2c.Sprc.Sin.
7  Prc‘ In
, rc. § PI>>>»——> ‘ “(I

Sp:-c.Dext. & Sin.

Mesonephric Vlbuthries

l 2 Pc. Dext.

Fig. 12 Diagram of the venous system in the lumbar region of a 17-mm. sheep embryo, Harvard Embryological Collection, series 2118. Section I is from section 1449 of this series.

ively, the pars supracardinalis (P.Sprc.) and the pars renalis (P.Ren.), which make up the postrenal portion of the Vena cava in the adult sheep. As regards its embryonic components, therefore, the posterior vena cava in the sheep, throughout its entire length, is identical with the vena cava in the pig, the cat, and in man. DEVELOPMENT or THE POSTERIOR VENA CAVA 309

Signiﬁcance of the variations in the venous system among the foregoing sheep embryos

The question now arises, do the venous systems in these four sheep embryos of from 14 mm. to 17 mm. (ﬁgs. 9, 10, 11, and 12) represent typical stages in the development of the veins in the sheep, or do they represent unusual, aberrant conditions peculiar only to these particular embryos“! A complete and correct answer to this question could be given only after careful examination of a far greater number of embryos between these ages than has been studied during the course of this investigation. However, with the evidence at hand, gained from a study not only of the embryos described, but also of others of approximately the same ages, we may assume that the course of venous development in the sheep between 14 mm. and 17 mm. in length is subject to marked individual variation. In the sheep, as in Didelphys, variation seems to be the rule. Moreover, whether the condition in these sheep embryos be typical or atypical, the fact remains that all the venous channels which they possess can be correlated with the veins in other mammals and with a common mammalian venous plan. From the standpoint of comparative embryology, this is the important fact.

In all mammalian embryos studied, the development of the venous system in the lumbar region takes place through a successive utilization of three pairs of longitudinal channels, the posterior cardinal (Pc.), subcardinal (Saba), and supracardinal (Spra) and the various cross anastomoses between them. All these three primary channels, or evidences of them, are present, so far as is known, in the embryos of all placental mammals. Differences in venous development among different species of mammals are due to variations in the relative functional roleiwhich these veins play during the course of development. In some mammals, notably in the pig and in the sheep, other veins appear and play an auxiliary’ role for longer or shorter periods of development, but do not contribute directly to the formation of the adult system. In the pig these temporary veins are the ventral 310 ELMER G. BUTLER

vein of the mesonephros (VAL, ﬁgs. 2, 3, and 4), which for a time is as prominent as either the posterior cardinal or subcardinal Vein, and the lateral vein of the mesonephros (V. M es.Lat., ﬁgs. 4 and 5), a temporary drainage vein for the hind-limb bud and the caudal end of the body. Moreover, in pig embryos of from 14 mm. to 17 mm. it is not unusual to ﬁnd a prominent vein along the ventromedial border of the caudal half of each mesonephros. This vein, when present, is usually a drainage vein of the mesonephros only, though in some embryos it aids also in the drainage of the hind limb and caudal region of the body. In the sheep, the same Ventromedial vein of the mesonephros (Subc.Vent., ﬁgs. 9 and 11) is frequent in occurrence and, as we have seen, often plays a very prominent role in the drainage of the hind limbs and the caudal end of the body. A lateral vein of the mesonephros (V.Mes.Lat., ﬁgs. 9 and 11), similar in location and function to that in pig embryos, is often found in the sheep; however, in the latter, it appears to be always smaller and of less functional signiﬁcance than in the pig. Also classed among the vessels auxiliary to the posterior cardinal, subcardinal, and supracardinal veins is the cardinal collateral vein (C.C., ﬁg. 11). As suggested above, the cardinal collateral vein is a part of the general subcardinal pathway. In those cases where circumumbilical venous rings are present, the ventral half of each ring is formed by the caudal continuation of the cardinal collateral vein.

Figure 13, which represents an idealistic cross section through the lumbar region of pig and of sheep embryos, is designed to illustrate the typical positions and relations of the veins referred to in the preceding pages, namely, the posterior cardinal (Pa), the subcardinal (Suba), the supracardinal (Sprcn), the lateral vein of the mesonephros (V.M es. Lat.), the ventral vei11 of the mesonephros (V.v.), the ventromedial vein of the mesonephros (Subc.Vent.), and the cardinal collateral vein (C.C.). The presence of three of these veins, the lateral vein of the mesonephros, the ventral vein of the mesonephros, and the ventromedial vein of the DEVELOPMENT or THE POSTERIOR VENA CAVA 311

mesonephros, is clearly due to the large size and the great functional importance of the mesonephroi in embryos of the pig and the sheep; they have not been found in embryos of these mammals in which the mesonephroi are relatively small and of much less functional signiﬁcance. The posterior cardinal, the subcardinal, and the supracardinal veins, developed to a greater or lesser degree, are found in the embryos of all species of mammals investigated. The posterior cardinal is always the ﬁrst to appear; the subcardinal and the supracardinal are established later as auxiliary veins to the posterior cardinals, and during the later course of development they frequently supplant the posterior cardinal veins entirely.




Pc,Dm.l Pr 5-»A ' ‘ C.C.Du\. C.C Sm S..b=.Dut. I"! \“I 5...‘ s. V. Mu Lnt Du-v.. v M“ Ln 5 ,

s«.s¢.\«-ya nut. 5”,‘ VM 5.“ Vv Dul. V». Sm

Fig. 13 An idealistic cross-section through the lumbar region of a pig or a sheep embryo, showing all of the potential venous channels. For this diagram the writer is indebted to Prof. C. F. W. McClure.

DEVELOPMENT OF THE POSTERIOR VENA CAVA IN THE BAT (MYOTIS LUCIFUGUS, LE CONTE)“

The chief investigation which has preceded this study of the Veins in bat embryos is the beautiful and comprehensive research. of Grosser (’01), which includes both the anatomy and the development of the entire vascular system of the Chiroptera. With respect to the development of the posterior vena cava in the Microchiroptera, Grosser’s conclusions are essentially the same as those drawn by Hochstetter (’93) concerning the development of the cave in the rabbit. Grosser

’ No record of the species of bat embryos used in this investigation was made when the embryo were taken. Considering the locality in which they were collected (State of Indiana)‘, they are probably all Myotis lucifugus, LeConte. 312 ELMER G. BUTLER

states (p. 361) that “Die Entwickelung dieses Gefasses weicht nur in einigen Details von der beim Kaninchen ab.” In following pages the writer will attempt to show that the type of development of the posterior vena cava in the bat appears to correspond rather more closely to that found in the cat, in man, and in the pig than to that of the rabbit. Although this conclusion and others which may be drawn from the present study differ from those of Grosser, the writer fully appreciates and acknowledges the value of this previous investigation.

The accompanying diagrams (ﬁgs. 14, 15, 16, 17, 18, and 19) illustrate the successive stages in the development of the posterior vena cava in the bat, from the early cardino— subcardinal venous plan to the adult condition. Careful examination of these six diagrams will serve to give the reader a general understanding of the transformations which the venous plan undergoes in the establishment of the adult posterior vena cava and its tributaries. A description of each individual stage will not be given; rather in the following discussion an attempt will be made to point out only the more salient features of development, of particular importance from the standpoint of comparative embryology.

As in all mammals thus far investigated, the plan of the cardinal venous system in young bat embryos (fig. 14) consists of three pairs of bilaterally symmetrical veins, the anterior cardinal (Prc.Deact. and Sin.), the posterior cardinal (Pc.De9ct. and 82%.), and the subcardinal (Subc.). On each side of the body anterior and posterior cardinal veins unite to form the common cardinal vein (D.C'.) which opens into the sinus venosus. Subcardinal (Saba) and posterior cardinal (Pc.) veins are connected at intervals by subcardinoposterior cardinal anastomoses (Amzst.Subc.Pc.). Such a cardinal venous plan represents the elementary embryonic arrangement common to all sauropsida and mammalia, so far as known, and has been termed by Huntington and McClure (’20) the cardino-subcardinal stage. DEVELOPMENT or THE POSTERIOR VENA CAVA 313

The ﬁrst critical modiﬁcation (ﬁg. 15) of this elementary, symmetrical ground plan occurs as the result of the formation of the hepato-subcardinal junction (Hep.Subc.Jct.). This junction, taking place by way of the caval mesentery, between the right subcardinal vein and the liver sinusoids, is established in bat embryos at a relatively early stage of development, namely, at about 5 mm. in length. The formation of the hepato-subcardinal junction marks the establishment of the prerenal division of the posterior vena cava, composed, as in all mammals, of two main embryonic subdivisions, a pars hepatica (P.Hep.), which is the portion of the vena cava lying cranial to the hepato-subcardinal junction, and a pars subcardinalis (P.Subc.), the part of the prerenal division of the cava caudal to the hepato-subcardinal junction. The pars hepatica (P.Hep.) is formed from the vena hepatica communis of Hochstetter, liver sinusoids, and an independent vein within the caval mesentery; the pars subcardinalis

represents a portion of the right subcardinal vein (P.S’ubc.,_

Subc.Dext.).

Following the formation of the hepato-subcardinal junction (ﬁg. 15), one of the right subcardino-posterior cardinal anastomoses (A%ast.Subc.Pc.*) becomes greatly enlarged, so that blood from the right side of the body in the lumbar region is diverted to the heart by way of the prerenal division of the vena cava (P.Hep.andP.Subc.). As a result of this shift in blood ﬂow, the right posterior cardinal vein (Pc.Dewt.) between the mesonephros .and the right common cardinal vein (D.(7.) shrinks in size and soon becomes discontinuous (ﬁg. 16). Following this change, all the blood from the caudal half of the right side of the body passes to the heart by way of the prerenal division of the vena cava. On the left side of the body, however, blood still continues to pass through the

left posterior cardinal vein (Pc.Sin.) and into the heart by way of the left common cardinal vein (D.C.).

Such a condition of asymmetry in embryos of the bat (ﬁg. 16), i.e., the condition in which the left posterior cardinal vein (Pc-Sm.) throughout its entire length remains con314 ELMER G. BUTLER

ti11uous and of prominent functional importance after the right posterior cardinal Vein (Pc.Deact.) has disappeared in its middle third, is due to the virtual absence in bat embryos of an intersubcardinal anastomosis. In embryos of all other mammals thus far investigated a prominent anastomosis between the subcardinal veins caudal to the level of the

P”. out

Pc. Dext.

Fig. 14 The cardino-subcardinal venous plan cllaracteristic of all young mammalian embryos. DEVELOPMENT OF THE POSTERIOR VENA CAVA

omphalomesenteric artery is formed nearly coincident with the establishment of the hepato—subcardina1 junction; blood from the left side of the body is then diverted through this intersubcardinal anastomosis and into the prerenal division of the Vena cava. In bat embryos this does not occur; only

prc. Sin

PC. Sin.

Fig. 15 Diagram of the venous system of a 5-mm. bat embryo, Princeton Embryological Collection, series 1661.

THE AMERICAN JOURNAL or ANATOMY, von. 39, N0. 2 316 ELMER G. BUTLER

a Very ﬁne capillary plexus of veins appears between the right and the left subcardinal Veins. This capillary intersubcar~ dinal anastomosis of the bat never attains any great size and





Prc.Dext. Pro. Sin. PC Dext ‘:4 pc. Sin. H6P.5ubc.Jc‘L 2.24

I-\.0m. Anast, Subs. Sprc. Sin.

Anast. Sui:-c. Pc.

P.SuLc.(Subc.Daxt. ‘V - AnasLSu|:c.Pci.(' .

Anast. Subc. Sp:-:.D¢xt (P. Ran)

Sub:.Daxt.

I6


V"""is";'n...s;.. 9..s-.§.f '

Fig. 16 Diagram of the venous system of a 5.5-mm. bat embryo, Princeton Embryological Collection, series 1662. Section J is from lide 8, section 10, of this series. DEVELOPMENT OF THE POSTERIOB VENA CAVA 317

assumes no marked functional importance. It is, indeed, usually traced with difficulty as a complete intersubcardinal connection; hence it can play no part in directing the blood ﬂow from the left side of the body into the prerenal division of the vena cava. Because of its small size and its functional



Pc.Sin. Hep.Subc.Jcl.. P. subc... Spy-c.Sm Amt. sue. PST Km ) Angst Int Sprcixh P.Ren. ‘,‘f (‘((«K (Anastsuluc. Sp:-c.) I : ’ A,.351__ $u|,.;_P¢, 5ul:c.Dext. ' 1 ' Anasl’..5ul>c.Sprc. Sin.



A. Um la. Dext. V.I l. In. Dexl.

Anast.Il. Pc.

I 7

Fig. 17 Diagram of the venous system in the lumbar region of a 6.5-mm. bat embryo, Princeton Embryological Collection, series 1664. Section K is from slide 8, section 37, of this series.

unimportance, any indication of an intersubcardinal anastomosis has been omitted from the accompanying diagrams.

Not only is the intersubcardinal anastomosis a negligible factor in bat embryos, but also the subcardinal veins themselves, with the ‘exception of that part of the right subcardinal Vein (P.Subc., Subc.Deact.) which enters into the forma318 ELMER G. BUTLER

tion of the vena cava, play a far less important role than is often the case in mammals. The subcardinal veins in bat embryos never attain any great size and they never function as the chief drainage vessels of the mesonephroi as they do, for example, in pig and in human embryos. The history of the lumbar subcardinal veins in the bat is similar to their history in cat embryos; in both of these mammals lumbar subcardinal veins disappear as continuous channels relatively early, while the lumbar posterior cardinal veins increase i11 size and persist until a comparatively late stage of development as the principal drainage veins of the caudal portions of the mesonephroi.

Soon after the establishment of the prerenal division of the posterior vena cava, small capillary supracardinal veins appear on each side of the body in the lumbar region. In a bat embryo of 5.5 mm. (ﬁg. 16) each lumbar supracardinal vein (Sprc.De0ct. and Sin.) connects With the corresponding posterior cardinal vein (Pc.Deact. and 81%.)» just cranial to the umbilical artery. and from this point extends anterior to about the level of the omphalomesenteric artery. On each side of the body, subcardinal (Saba) and supracardinal (Spra) veins" are connected by several small subcardino— supracardinal anastomoses (Anast.Subc.Sprc..Deact. and Sin.). The most prominent of these anastomoses is the most anterior, and on each side of the body it is this anastomosis which persists in later stages of development; the more caudally situated subcardino—supracardinal anastomoses disappear with the obliteration of the subcardinal Vein and are not found in older embryos.

Identiﬁcation of capillary supracardinal veins at this early stage of development indicates rather clearly that these veins must be considered as a new pair of vessels, separate and distinct from the posterior cardinal veins. They are certainly not formed by a splitting of the posterior cardinals, which at this stage still occupy positions dorsal to the mesonephroi and lateral to the migrating kidneys; rather, each supracardinal vein appears to have arisen through a longitudinal DEVELOPMENT on THE POSTERIOR VENA CAVA 319

coalescence of a number of venous tributaries from the dorsal body wall, which extend round the dorsomedial side of the kidney and open into the subcardinal vein. Supracardinal veins in the bat appear to be identical in origin, in -location, and in the developmental role which they play with the same



V. I l. Ex. Dext.

V.I|.In. Com. V.I|.In. But.

I 8

Fig. 18 Diagram of the venou system in the lumbar region of an 8-mm. bat

embryo, Princeton Embryological Collection, series 857. Section L is from slide 15, section 8, of this series.

channels in cat, man, pig, and sheep. In the bat,'as in these other mammals, the appearance of the supracardinal veins and the subcardino-supracardinal anastomoses marks the establishment of the postrenal division of the posterior vena cava. On. the right side of the body the right subcardinosupracardinal anastomosis (Anast.Subc.Sprc.Dea;t.) and the right supracardinal vein (Sprc.Deact.) form, respectively, the 320 ELMER G. BUTLER

pars renalis (P.Ren.) and the pars supracardinalis (P.Sprc.) of the adult Vena cava.

The establishment of the lumbar supracardinal Veins and the subcardino-supracardinal anastomoses results in the formation on each side of the body of a large perimetanephric venous ring encircling the entire kidney. This ring in a bat embryo of 5.5 mm. (ﬁg. 16) is identical with the perimetanephric venous ring previously described in human embryos of 15 mm. (McClure and Butler, ’25, ﬁgs. 7 and 9). In both cases the medial side of the perimetanephric ring is composed of the lumbar supracardinal Vein (Spra) and the subcardino-supracardinal anastomosis (Anast.Subc.Sprc.); the lateral side is made up of the lumbar posterior cardinal Vein (Pc.) and a subcardino—posterior cardinal anastomosis (Anast. Subc.Pc.). In older bat embryos (ﬁg. 17), following further cranial migration of the kidney, each perimctanephric Venous ring becomes much smaller in diameter and forms a rather small, compact ring which encircles the ureter; it becomes, in other words, a typical periureteric Venous ring. This decrease in size of the large perimetanephric venous ring to form the small periureteric ring appears to be due, for the most part, to an increased growth of each of its component parts, especially of the supracardinal Vein and the subcardino—supracardinal anastomosis.

By the time the 6.5—mm. stage (ﬁg. 17) is reached, both lumbar supracardinal Veins have increased greatly in size and are prominent drainage channels for the hind—limb buds and the caudal end of the body. On each side of the body in a 6.5-mm. bat embryo the supracardinal Vein is approximately the same size as the corresponding posterior cardinal vein, both supracardinal and posterior cardinal vessels on the right side being larger than those on the left. Accompanying the growth of the supracardinal Veins has been a corresponding increase in size of the subcardino-supracardinal anastomoses

(Anast.Subc.Sprc.De:ct. and Sin), with the result that they, also, are much more conspicuous and important channels than at the 5.5-mm. stage. The most important change, however, DEVELOPMENT OF THE POSTERIOR VENA CAVA

which accompanies the growth of the supracardinal Veins is the formation of several anastomoses (Anast.Int.Sprc.) dorsal to the aorta between the right and the left supracar— dinals. The largest of these intersupracardinal anastomoses (Ana,st.Irnt.Sprc.*) lies at the level of the right and the left subcardino—supracardinal anastomoses. In the 6.5-mm. bat these three anastomoses (i.e., the intersupracardinal and the



. Is‘ Pc.Déxt '| -I 1 :

3 5 3’ $ul>c.Dext : ”l, '_E_.pc Sm Hep.Sul>c.Jct. /_L....—_—,.—,——5..l,¢ 5,"

Ren.Dext. ” '

Sm. Sin P. Suhc. _ _ _ _ _ _ _ P Ren R¢n.$in.

(A..ast.s'..1.¢ .59....

I9

Fig. 19 Diagram of the posterior vena cava of an adult bat

right and left subcardin0—supracardinal anastomoses) form a broad Venous band which passes round the dorsal side of the aorta and serves as the main connecting channel between the Veins of the left and the right sides of the body.

Appearing at approximately the same level (actually, slightly more caudal) as that at which the intersubcardinal anastomosis is usually located, and bearing the same relation to the subcardino—supracardinal anastomoses, the int.ersupra322 ELMER G. BUTLER

cardinal anastomosis (Anaist.Int.Sprc.*) in bat embryos plays the same functional role as does the intersubcardinal anastomosis in embryos of other mammals; it serves to direct the blood from the left side of the body into the prerenal division of the posterior vena cava. As a result of this shift in blood ﬂow, the left posterior cardinal vein (Pc.Sm.) between the mesonephros and the left common cardinal vein becomes discontinuous; all of the blood from both sides of the body caudal to the level of the hepato-subcardinal junction in bat embryos of 6.5 mm. passes to the heart by way of the prerenal division of the vena cava (P’.Hep. and P.Subc.). Eventually, the intersupracardinal anastomosis (Amzst.Int.Sprc.*), as does the intersubcardinal anastomosis in other mammals, enters into the formation of the left renal vein in the adult bat, which passes dorsal instead of Ventral to the aorta.

At this point it will be of interest to digress slightly in order to consider the comparative development in different mammals of the so—called "renal collar.’ In embryos of the cat (Huntington and McClure, ’20) the intersupracardinal anastomosis forms the dorsal side of a complete venous ring, the renal collar, which encircles the aorta caudal to the omphalomesenteric artery (ﬁg. 26) ; ventrally, the renal collar is made up of the intersubcardinal anastomosis, and on each side of the subcardino—supracardinal anastomosis. In human embryos we ﬁnd that the dorsal, intersupracardinal component of the renal collar is usually poorly developed, while in pig and in sheep embryos the dorsal side of the renal collar seems invariably to be lacking. In embryos of the bat, on the other hand, we now ﬁnd that it is the dorsal, intersupracardinal component of the renal collar which is always present and is always of prominent importance, while the ventral, intersubcardinal component is either poorly developed or entirely absent. The recognition of a complete renal collar, as found in embryos of the cat, is of great Value in interpreting properly the conditions in other mammals. A complete venous ring encircling the aorta may be considered as the fundamental groundplan; the conditions in human, pig, DEVELOPMENT on THE POSTERIOR VENA CAVA 323

sheep, and bat embryos are merely different variations of this plan.

During the course of development in the bat between the ages of 6.5 mm. and 8 mm., both lumbar posterior cardinal veins disappear, so that the continuity of the right and the left periureteric venous rings is broken. In an 8-mm. bat embryo (ﬁg. 18) all the blood from the hind-limb buds and the caudal end of the body passes through the two lumbar supracardinal veins, both of which have become markedly larger than they were at the 6.5-mm. stage. The right supracardinal vein (P.Spr0., Sprc.Dea0t.) and the right subcardino—supracardinal anastomosis (P.Ren.,Anast.Subc.Sprc.), in other words, the pars supracardinalis and the pars renalis of the vena cava, now form the direct caudal continuation of the prerenal division of the cava (P.Hep. and P.Subc.), so that throughout its entire length the posterior Vena cava is now the main venous channel of the body, having virtually attained its adult condition. The left lumbar supracardinal vein (Sprc. Sm.) in 8-mm. embryos is about one-half the caliber of the right supracardinal (P.Sprc.,Sprc.Deact.) and serves principally as the cranial continuation of the left external iliac vein. _

In an 8-mm. embryo (ﬁg. 18) the mesonephroi and gonads have been displaced far lateral in the abdominal cavity by the migration and growth of the permanent kidneys (metanephroi). The mesonephros and gonad on each side of the body are drained by a vein of relatively small caliber (Anast. Subc.Pc.) which passes mediad across the ventral surface of the kidney. On the right side of the body this vein opens into the pars subcardinalis of the vena cava; on the left side, into the left subcardino-supracardinal anastomosis. Each of these mesonephric and gonadial drainage veins in the 8-mm. embryo represents, in a somewhat modiﬁed form, the subcardinoposterior cardinal anastomosis which, up to this stage, formed a portion of the periureteric venous ring-. During the course of later development, these veins become transformed into the right and the left sex veins of the adult bat. 324 ELMER G. BUTLER

Bat embryos of 8 mm. (ﬁg. 18) possess deﬁnite renal veins on each side of the body. The right renal vein (Ren.De9ct.) passes from the right kidney, which has migrated to a position relatively far anterior in the abdominal cavity, directly into the pars subcardinalis (P.Subc.) of the posterior Vena cava. The left kidney, occupying a position much posterior to that of the right, lies with its hilum opposite the left subcardino— posterior cardinal anastomosis, into which the left renal Vein (Ren.Sin.) opens. Right and left renal Veins may at times be double instead of single.

The transformations through which the iliac Veins have passed in establishing the conditions found in embryos of 8 mm. (ﬁg. 18) can best be understood by a comparison of ﬁgures 16, 17, and 18. It is particularly noteworthy that in the bat the external iliac veins (V.Il.E:v.Dewt. and sm.) when they first appear, do not open into the iliac anastomosis of the posterior cardinals (AmLst.Il.Pc.), as they do, for example, in cat, man, pig, etc.; rather they open directly into the posterior cardinal Veins somewhat anterior to the level of the umbilical arteries (ﬁg. 17). Later (ﬁg. 18), after the loss of the lumbar posterior cardinal veins, each external iliac opens directly into the supracardinal Vein at the point where the posterior cardinal and supracardinal originally joined. The common internal‘ iliac Vein (V.Il.In».C0m.) of 8—mm. embryos, into which empty the internal iliac and caudal veins, is formed from the iliac anastomosis of earlier embryos, together with the portion of the right posterior cardinal vein between this anastomosis and the supracardinal.

Study of embryos older than 8 mm. shows that the transformation of the posterior Vena cava and its tributaries from the condition in 8—m1n. embryos (ﬁg. 18) to that of the adult bat (ﬁg. 19) is the result of relatively few alterations. The chief of these is the loss of the left lumbar supracardinal Vein (Sprc.Sm.). Following the loss of this Vein, the left external iliac vein (V.Il.Eoc.S-in.) opens directly into the pars supracardinalis of the Vena cava, passing dorsal to the aorta by way of what was originally an intersupracardinal anastoDEVELOPMENT on THE POSTERIOR VENA CAVA 325

mosis (Anast.Imt.Sprc.). In the adult the common internal iliac vein (V.I§.In.Com.) is retained in practically the same form as it occurs in embryos of 8 mm.”

The renal veins of the adult bat (ﬁg. 19) are probably identical with those in 8-mm. embryos. In any case, there has been little change. The right renal vein of the adult (Ren.Dewt.) opens into the Vena cava at a point rather far anterior to the left renal vein. The left renal vein (Ren. Sim), made up of three embryonic components, the intersupracardinal anastomosis, the dorsal part of the left subcardino-supracardinal anastomosis, and the vein between this anastomosis and the kidney, lies dorsal to the aorta and joins the cava about midway between the left external iliac vein and the right renal vein.

Sex veins (V.S.I.Deoct. and Sin.) in the adult bat represent the persistence, in a somewhat modiﬁed form, of the mesonephric and gonadial drainage veins of the 8—mm. embryo. The left sex vein joins the left renal vein.

Summary

Development of the posterior vena cava in the bat conforms closely to the type of development found in other mammals which possess prominent lumbar supracardinal veins. Differences in development which the bat exhibits are associated principally with the slight réle played by the subcardinal veins, the absence of an intersubcardinal anastomosis, and the substitution for it functionally of a prominent intersupracardinal anastomosis which lies dorsal to the aorta. Such a variation in the role of embryonic veins and their cross an.astomoses results in variations in the arrangement of the tributaries of the adult vena cava, particularly the left renal vein. In the adult bat we have an interesting illustra ‘° In one species of bat (Rhinolophus hippoiderus) Grosser (’01) reports that the left external iliac vein opens intopthe Vena cava in common with the left renal vein. Such a condition is undoubtedly due to the persistence of the left lumbar supracardinal vein as the proximal part of the adult external iliac; it is readily interpretable by reference to ﬁgure 18. 326 ELMER G. BUTLER

tion of the fact that what is the typical condition of the venous system in one adult mammal may be identical with the atypical condition in another.

DEVELOPMENT OF THE POSTERIOR VENA CAVA IN THE RAT

The development of the posterior vena cava in the rat follows a course far simpler than that in other mammals thus far investigated. Indeed, the development is of so elementary a type that a knowledge of the embryology of the venous system in the rat alone would serve to give a very meager understanding of the general plan of development of the mammalian vena cava. The rat, it may be said, represents the extreme in the possession of a simple type of development of the posterior vena cava.

The single contribution which has preceded this study of the development of the vena cava in rat embryos is a brief abstract by Begg (’16). In this abstract Begg states that below the diaphragm there is no supracardinal system of veins; that the vena cava of the adult rat caudal to the level of the renal veins represents the persistent right posterior cardinal vein. In all essential respects the observations of the writer verify these statements. However, as will be pointed out later, although lumbar supracardinal veins in the form of prominent longitudinal channels corresponding to those in other mammals do not appear in the rat and play no part in the development of the vena cava, nevertheless, there is, during a certain period of development, a deﬁnite supracardinal plexus of veins in the lumbar region of rat embryos.

The following discussion, illustrated by a series of ﬁve diagrams (ﬁgs. 14, 20, 21, 22, and 23) taken from reconstructed embryos, deals with the more important transformations through which the embryonic veins in the rat pass in establishing the adult posterior vena cava and its main tributaries. To avoid needless repetition, the writer will pass over as brieﬂy as possible transformations in the rat which are virtually identical with those in other mammals previously considered; transformations which vary from those of other mammals wi.ll be dealt with more fully. DEVELOPMENT or THE POSTERIOR VENA CAVA 327

Before considering the steps in venous development, the reader’s attention must be directed to the extremely small size of the mesonephroi in rat embryos. It has already been noted that in embryos of other mammals, particularly the pig and the sheep, the size of the mesonephroi is the most obvious and probably the most important factor inﬂuencing the course of venous development. In rat embryos the mesonephroi are exceedingly small organs, and, moreover, as Bremer ( ’16) has pointed out, mesonephric glomeruli never develop, which indicates that the mesonephroi undoubtedly remain functionless throughout the course of development. The problem, therefore, of the venous drainage of these organs in embryos of the rat is a negligible one. Hence, posterior cardinal veins are never so closely associated with the mesonephroi as in those mammals in which these organs are large and functionally active. Rather, the chief function of the posterior cardinal Veins throughout the course of development in the rat is the drainage of the dorsal body wall, the hind-limb buds, and the caudal region of the body.

The plan of the venous system in young rat embryos, as in the early embryos of other mammals, is of the simple cardinosubcardinal type (ﬁg. 14), consisting of anterior cardinal (P7’0.), posterior cardinal (Pc.), and subcardinal (Subc) veins. This elementary venous groundplan is present in rat embryos of approximately 7 mm. in length.

The hepatdsubcardinal junction (IIcp.Su—bc.Jct.), the ﬁrst important modiﬁcation of the cardino—subcardinal plan, appears between the ages of 7 mm. and 9 mm. Immediately following its formation the right subcardinal vein caudal to the hepato-subcardinal junction increases rapidly in size and forms a prominent connection with the right posterior cardinal vein at a point just caudal to the level of the omphalo— mesenteric artery. The right subcardinal vein (P.Subc., Subc.I)iea:t.) and the lumbar portion of the right posterior cardinal vein (P.C'ard., Pc.Dext.) then form the main venous channel in the right side of the body. Such a condition is found in embryos of 8.5 mm. and 9 mm. (ﬁg. 20). 328 ELMER G. BUTLER

The formation of the hepato-subcardinal junction in the rat marks the establishment of the posterior vena cava not, as in other mammals, in its prerenal division only, but throughout its entire length. The right posterior cardinal vein, caudal to its junction with the right subcardinal, persists throughout all stages of development and eventually forms the postrenal division of the vena cava. In its entirety, therefore, the pos terior vena cava of the rat, as it is marked out in embryos of 8.5 mm. and 9 mm. (ﬁg. 20), is made up of three embryonic components: a pars hepatica (P.Hep.), a pars subcardinalis (P.Subc.), and a pars cardinalis (P.Ca,rd.). The ﬁrst two, the pars hepatica and the pars subcardinalis, which comprise the prerenal division of the cava, correspond with the same parts in other mammals, while the pars cardinalis in the rat takes the place of both the pars renalis and the pars supracardinalis in the cat, man, pig, sheep, and bat.

After the formation of the hepato—subcardinal junction, all further transformations consist primarily in a series of modiﬁcations which bring about a general shift of the blood ﬂow from all parts of the body caudal to the liver into the main caval channel. The intersubcardinal anastomosis (Amtst.Im£. Saba), at ﬁrst plexiform in character, is established between the ages of 9 mm. and 10 mm. By way of this anastomosis, blood passeslvfrom the left side of the body into the vena cava, with the result that the left posterior cardinal (Pc.Sz'n.) shrinks in size and in 10-mm. embryos (ﬁg. 21) is no longer a continuous channel to the common cardinal vein. Since the right posterior cardinal vein (Pc.Dea:t.) loses its continuity at an even earlier stage, shortly after the appearance of the hepato-subcardinal junction, all of the blood from the l.umbar and caudal regions of the body in embryos of 10 mm. passes to the heart through the posterior vena cava.

The iliac anastomosis between the posterior cardinal veins (Amtst.Il.P‘c.) appears about coincident with the establishment of the intersubcardinal anastomosis. After its formation, an increasingly greater amount of blood from the left hind-limb bud and the tail region of the embryo passes DEVELOPMENT OF THE POSTERIOR VENA CAVA

Pc. Dext.


P. Card.(Pc.Dc><'t.)

P=.Dut. P. SuE¢I(su5:.De)<t.)

2 O Subc.'Sin.

A.0m.

Fig. 20 Diagram of the venous system of 8-mm. to 9-mm. rat embryos. Section M is from an 8.5-mm. (14 days) 1-at embryo, Embryological Collection of the College of Physicians and Surgeons (Columbia. University), series 873, slide 11, section 25. 330 ELMER G. BUTLER

into the pars cardinalis (P.Ccwd.) of the vena cava. As a result, the left lumbar posterior cardinal vein (Pc.Sm.) shrinks in size, and in 10-mm. embryos (ﬁg. 21) it has barely one—half the caliber of the vena cava.

Between the ages of 10 mm. and 11 mm. the kidneys (metanephroi) pass out from within the umbilical arteries and occupy positions directly ventral to the posterior cardinal veins (ﬁg. 21, section N). As cranial migration continues, each kidney passes lateral to the cardinal vein, forcing the vein somewhat mediad and pressing it between the medial side of the kidney and the aorta (ﬁg. 22, section 0). This relation of kidney and cardinal vein in the rat is of prime signiﬁcance. In no other mammal thus far studied does the migrating kidney pass lateral to the main cardinal channel. Usually, the kidney passes medial to the posterior cardinal vein, thereby occupying a position between the vein and the aorta; this is shown particularly well in cat, human, and bat embryos. This variation between the rat and other mammals, as regards the relation of the kidney a.nd cardinal vein, is due, certainly to a great extent, to the dissimilarity in size and importance of the mesonephroi, In those mammals which possess prominent and functionally active mesonephroi, each cardinal vein (or its derivatives) remains throughout development closely associated with the mesonephros, and therefore the cardinal vein‘ is always lateral, or, as in later stages, ventrolateral to the kidney. In the rat, on the other hand, cardinal veins are never closely bound to the extremely small and probably functionless mesonephroi. As the kidney advances craniad the posterior cardinal vein and mesonephros readily separate, allowing the kidney to pass between, medial to the mesonephros and lateral to the cardinal vein. In the rat there is never the slightest indication of a periureteric venous ring. _

Up to the age of 9 mm. segmental veins on each side open into the posterior cardinal vein as a series of Vessels separate and distinct from one another and independent from the segmental veins on the opposite side of the body. After the DEVELOPMENT or THE POSTERIOR VENA CAVA 331

9-mm. stage, however, this simple arrangement does not long persist. Between the ages of 9 mm. and 10 mm. appear a series of irregular cross anastomoses between the segmental veins of the ri.ght and the left sides of the body in the region just ventral to the developing central of the vertebrae. These irregular cross anastcmoses, between the segmental veins of the two sides, also anastomose with each other, particularly in the region between the sympathetic nerves, so that the result is a closely interwoven venous plexus (labeled Sprc. in section N, ﬁg. 21) along the dorsal side of the aorta. Such a plexus is clearly distinguishable in 10-mm. and 11-mm. embryos. At intervals this dorsal plexus (_Sprc.) connects with the posterior cardinal Veins (.Pc.Deaot. and Sin.) by way of small vessels which represent the proximal ends of the originally independent segmental veins. In the region anterior to the level of the intersubcardinal anastomosis, where cardinal veins are no longer continuous channels, a series of vessels passes from the dorsal plexus lateral to the aorta and on each side empty directly into the subcardinal vein.

The origin of the .supracardina1 venous plexus in rat embryos and its location dorsal to the aorta clearly indicate that this plexus is entirely homologous with the supracardinal plexus which in other mammals precedes the formation of prominent lumbar supracardinal veins. However, since in the rat lumbar posteriorcardinal veins always lie close to the aorta and are not displaced laterally by the migration of the kidneys, and since the right posterior cardinal vein persists throughout all stages of development and eventually becomes a part of the vena cava, the ﬁnal transformation of the supracardinal plexus into right and left supracardinal veins never occurs in the lumbar region of the rat, as in other mammals. It is highly probable that the lumbar supracardinal plexus in rat embryos is concerned in later stages of development with the formation of the adult lumbar veins, as, indeed, is probably the case with a‘ portion of the supracardinal plexus in all other mammals investigated; however,

-mm AMERICAN JOURNAL or ANATOMY, von. 39, N0. 2 332 ELMER G. BUTLER

the formation of lumbar Veins has not been. carefully followed during this investigation.

It is needless to dwell on the transformation of the Vena cava and its tributaries in embryos older than 11 mm. and 12 mm. These transformations may best be understood by a comparison of ﬁgures 22 and 23. The prerenal division of the posterior Vena cava in the adult rat is made up of a pars hepatica (P.Hep.) and a pars snbeardinalis (P.S’ubc.), iden '-'u 'u

s>c.oext.___3

I I c




Subs. Dext.

Hep. Sul>c.Jci..

P. 5ubc.(5ubr.Dexi,.) it

Fig. 21 Diagram of the venous system in the lumbar region of 10-mm. to 11—mm. rat embryos. Section N is from a 10-mm. (14 days, 12 hours) rat embryo, Embryological Collection of the College of Physicians and Surgeons (Columbia University), series 908, slide 12, section 3. DEVELOPMENT on THE POSTERIOR VENA CAVA 333

tical with the same components of the vena cava in other mammals; the postrenal division of the cava is entirely posterior cardinal (P.Cm"d.) in origin.

Deﬁnite renal veins appear ﬁrst in embryos of about 12 mm. (ﬁg. 22). The right renal vein connects directly with the pars subcardinalis of the vena cava; the left renal vein empties into the left side of the intersubcardinal anastomosis. In the adult (ﬁg. 23), the embryonic intersubcardinal anas



P. Subcisubc. Dext.)|"

Ren.Dext.

I

22

Fig. 22 Diagram of the venou system in the lumbar region of 11-mm. to 12-mm. rat embryos. Section 0 is from an 11-mm. (16 days) rat embryo, Embryological Collection of the College of Physicians and Surgeons (Columbia University), series 849, slide 20, section 32. 334 ELMER G. BUTLER

tomosis (A%ast.Int.Subc.) makes up the greater part of the left renal vein.

During embryonic development the gonads drain into the subcardinal veins (Saba) caudal to the intersubcardinal anastomosis. Hence, in the adult rat, the proximal parts of the right and the left sex veins (V.S'.I.Dea:t. and Sin.) represent portions of the embryonic subcardinals.

Suprarenal veins (Spr.Deact. and Sin.) in the rat differ in no essential respects, either in their development or in their adult condition, from those in other mammals.

Since in the rat the development of the posterior vena cava and its tributaries follows a course so simple and direct, it would be expected that the occurrence of atypical venous conditions in adult rats, due to variations appearing during the course of development, would be far less frequent than in such mammals as the cat and man where venous development is relatively much more complex. Such, indeed, appears to be the case. Examination of a large group of adult albino rats by C. F. Silvester, of the Princeton Laboratory, shows that the Venous system of the rat is of a very stable type and that it does not exhibit in the adult the variety of venous anomalies so frequently found in the cat and in man.

THE DEVELOPMENT OF THE POSTERIOR VENA (JAVA IN THE RABBIT

The development of the posterior vena cava in the rabbit has already been the subject of several investigations, chief among which are those of Hochstetter (’93) and of Lewis (’02). Lewis’s work demonstrates that the vena cava in the rabbit in its prerenal division is established in a manner essentially the same as has later been observed in other mammals investigated, but that the development of the postrenal division follows a course far simpler than that found in the cat, man, pig, etc. The postrenal division of the cava, according to the investigations of both Hochstetter and Lewis, is made up of two embryonic components: a short anastomosis between the right posterior cardinal and subcardinal veins DEVELOPMENT on THE POSTERIOR VENA CAVA 335

at the level of the intersubcardinal anastomosis and the lower part of ' the right posterior cardinal vein. However, the transformation of the right cardinal Vein into the Vena cava, as described by them, does not take place in the simple direct manner observed in rat embryos and described in preceding


Hep.$ul>c. Jet. i: P. Subc. ‘

Ren. Dext. A. Om V

Fig. 23 Diagram of the posterior vena cava in an adult rat

pages. The difference between the rabbit and the rat lies in the relation of the migrating kidney to the cardinal vein. In the rabbit the kidney during its cranial migration passes not lateral to the posterior cardinal vein as in the rat, but between the vein and the aorta, so that the ureter lies medial to the main cardinal trunk. According to Lewis, “from the shattered inner pieces of the cardinal vein, or from new offshoots 336 ELMER G. BUTLER

from the main stem, a venous connection forms on the median side of the ureter.” The result is a complete periureteric venous ring. As development progresses, the newly formed median loop of this ring increases rapidly in size and soon becomes the main channel,Awhile the part of the true cardinal trunk, which was forced lateral by the kidney, gradually becomes smaller and ﬁnally disappears.

Prominent periureteric venous rings are invariably present in rabbit embryos of around 13 mm. in length (ﬁg. 24). The lateral, posterior cardinal component of each ring (Pc.Deoot. and Sin.) bends sharply outward across the ventral side of the kidney, receiving a large tributary from the mesonephros (not shown in ﬁg. 24). The median half of each ring (Sprc. Deact. and Svm.), only slightly smaller than the lateral half, forms the shorter and more direct channel. All of the components of the posterior vena cava are already laid down, and at this early stage of development they can be most clea.rly distinguished. Cranial to the intersubcardinal anastomosis the vena cava is made up of a pars hepatica (P.Hep.) and a pars subcardinalis (P.Subc.), homologous with the same components in other mammals. Caudal to the intersubcardinal anastomosis the cava is also a composite vessel, consisting of the right subcardino—posterior cardinal anastomosis (Anast.Subc.Pc.Dext.), the portion of the cardinal vein (Pc.*) between this anastomosis and the periureteric ring, the median half of the ring (Sprc.De-a:i.), and the cardinal vein caudal to this ring (Pc.**). Although expressed in somewhat different language, this is essentially the conclusion of Lewis.

In all essential respects the observations of the writer conﬁrm those of Lewis. The point of difference is one of interpretation. Both Lewis and Hochstetter considered the median half of the periureteric ring as a part of the posterior cardinal line, and this would, indeed, appear to be the case if the rabbit alone be examined. However, in the light of observations on other mammals, the median half of this ring can be considered only as a part of the supraeardinal system. This is most easily and clearly demonstrated by a comparison DEVELOPMENT OF THE POSTERIOR VENA CAVA

of venous development in the rabbit and in the cat. In these two mammals venous development up to the appearance of the median_ loop of the periureteric ring is very nearly parallel. The venous system in the lumbar region of an 11-mm. rabbit, for example, is virtually the same as that in a 12-mm. cat embryo. In each the main cardinal channel bends sharply outward across the Ventral surface of the kidney, passing

5ubc.Dext..

Hep. 5ubc.Jcl’.. P. Sui->c.(Sub¢Dext.



Fig. 24. Diagram of the venous system in the lumbar region of a 13-mm. (15 days) rabbit embryo, Harvard Embryological Collection, series 158.

lateral to the ureter. The median side of the periureteric venous ring, although still incomplete, is far enough advanced in its formation so that in both the rabbit and the cat its location and its relation to other venous channels can be clearly noted. In each its location is identical; the difference is that in the cat the medial side of each periureteric ring is not isolated, but is a part of a developing, longitudinal venous trunk, the supracardinal vein, extending along the 338 ELMEB. G. BUTLER

aorta throughout both the lumbar and thoracic regions, while in the rabbit there is no such extensive supracardinal system of veins. Supracardinal veins in the lumbar region of the rabbit are restricted to the comparatively short areas of the periureteric rings. However, because of its origin, its location, and the role which it later plays, there can be no doubt but that the median half of the periureteric ring in the rabbit is precisely homologous with the median half of this ring in the cat. We can only conclude, therefore, that in the rabbit the median loop of the right periureteric ring, which contributes to the adult vena cava, is supracardinal in origin, and it has been so represented in ﬁgure 24.

The critical reader may here raise the objection that at the time when the median limbs of the periureteric rings ﬁrst appear in rabbit embryos, they are situated distinctly lateral to the aorta, and, therefore, are too ventral to be called a part of the supracardinal system of Veins, which is usually described as being located on each side of the body dorsolateral to the aorta and relatively close to the sympathetic trunks. The reply to this objection is that the right and the left lumbar supracardinal veins in the embryos of virtually all mammals vary in their location between the younger and the older stages of development. In the cat, for example, when supracardinal veins ﬁrst appear they are found lateral to the aorta. During the course of later development they come to occupy a more dorsal position, and the numerous intersupracardinal anastomoses which then develop between them form a broad venous plexus across the dorsal side of the aorta. A similar change in location of the lumbar supracardinal veins is shown particularly Well in bat embryos, and can be observed also in human and in pig embryos. Thus, the fact that the medial limbs of the periureteric rings in the rabbit are not precisely dorsolateral to the aorta does not excludethem from being considered as a part of the supracardinal system of veins. The designation, ‘supracardinal system of veins,’ as ﬁrst applied by Huntington and McClure and as subsequently used by them and other writers, is inDEVELOPMENT OF THE POSTERIOR VENA CAVA 339

tended to include, according to the interpretation of the present writer, the general venous pathway situated lateral and dorsal to the aorta, and often extending, as in the cat, throughout the lumbar and thoracic regions of the body. A careful comparison of the conditions in the cat, human, pig, and bat embryos with those in rabbit embryos cannot fail to convince one that the median half of each periureteric ring in the rabbit is a part of the supracardinal system of veins.

That the part of the right posterior cardinal vein (Pc.,* ﬁg. 24) cranial to the periureteric ring enters directly into the formation of the vena cava cannot be disputed. This has been clearly demonstrated by Lewis and is conﬁrmed by the observations of the writer. As the migrating kidney advances craniad from the region of the periureteric ring, it passes lateral to the cardinal vein, virtually separating the vein from the mesonephros. Thus the cardinal vein in this region remains relatively close to the aorta and is free to enter into the formation of the vena cava. Relations of kidney, cardinal vein, and mesonephros in a 14.5-mm. rabbit embryo are best shown in cross—section (ﬁg. 25). The situation is strikingly remindful of that in rat embryos, where the cardinal vein always lies medial to the kidney; but it is the exact opposite of the condition in all other mammals examined, in which the cardinal vein (or its derivatives) remains throughout development in intimate association with the mesonephros and occupies in older embryos a position lateral or ventrolateral to the kidney.

With respect to the relative importance of the posterior cardinal and supracardinal veins in the development of the vena cava, we may place the rabbit midway between the rat and other mammals, such as the cat and the pig. In the rat. posterior cardinal veins play the important role; supracardinal veins have no part in the formation of the cava. In the cat and the pig, on the other hand, we ﬁnd that it is the supracardinal system of veins which play the dominant role; posterior cardinal veins in these animals disappear and are not involved in the formation of the vena cava. In the rabbit 340 ELMER G. BUTLER

the postrenal division of the vena cava is about equally derived from the posterior cardinal and the supracardinal veins. Since venous development is closely linked with the activity of the mesonephroi, as has been shown in preceding pages, it might be expected that the variation in the development of the posterior vena cava in these different mammals is associated primarily with a dissimilarity among them in the duration of mesonephric activity.

Bremer (’16) has demonstrated that the size of the mesonephroi in a mammal cannot be taken as a direct index of their functional activity. He shows that, although young


Fig. 25 Cross-section through a 14.5-mm. (14 days, 18 hours) rabbit embryo, Harvard Embryological Collection, series 143, section 857.

rabbit embryos possess at ﬁrst rather large mesonephroi, there is little increase in their functional activity beyond the age of 9.6 mm. A rabbit embryo of 9.6 mm., for example, has about forty active glomeruli in each mesonephros. This increases only to forty-two glomeruli in an embryo of 14.5 mm. By the time the 21-mm. stage is reached, the organ has already begun to diminish; an embryo of this length possesses only thirty-four glomeruli in each mesonephros. That this is a relatively early stage for the degeneration of the mesonephroi is shown by the fact that in the pig the number of glomeruli becomes increasingly greater up to the 40-mm. stage,~and that in the cat the number of glomeruli increases steadily up to 39 mm. DEVELOPMENT or THE POSTERIOR VENA CAVA 341

This very striking correlation between venous development and mesonephric activity seems to the writer to be of prime signiﬁcance. That the type of venous development in the rabbit lies midway between that in the rat and that in the cat seems to be associated with the fact that, also in respect to the duration of mesonephric activity, the rabbit is midway between these two other mammals. The mesonephros in the rabbit probably reaches the peak of its functional activity at between 10 mm. and 11 mm., which means that from then on the task of the cardinal veins in draining the mesonephroi does not increase, but instead it gradually becomes less. Each posterior cardinal vein, therefore, becomes increasingly less closely associated with the mesonephros, and a portion of the right cardinal vein is free to enter into the formation of the posterior vena cava much as it does in the rat, where the posterior cardinal vein is never closely associated with the mesonephros. If it were possible experimentally to arrest mesonephric activity in the cat at the time and to the extent that it is normally arrested in the rabbit, we may suppose that the history of the posterior cardinal and the supracardinal veins would be the same in the cat as in the rabbit. On the other hand, if mesonephric activity steadily increased in the rabbit over a long period of time, as in the cat, then we might conﬁdently expect that the venous development would be the same in the rabbit as in the cat.

Such a point of view at once places on a new plane our understanding of the development of the vena cava in the rabbit and its correlation with the development in the cat. Not only do we recognize how the two are different, but also We understand, to some extent at least, why they are different. As will be shown in later pages, such a viewpoint toward the entire problem of the comparative embryology of the venous system reveals the subject in a new and a clearer light. 342 ELMER G. BUTLER

DISCUSSION

Although a detailed knowledge of the development of the posterior vena cava in each of the various mammals studied during the course of this investigation is in itself a matter of considerable interest and importance, the particular value of the present study lies in the fact that it enables us to draw clear and deﬁnite comparisons between different species, thereby interpreting the development in one mammal in the light of conditions found in other mammals. By such a method of comparison and correlation we gain not only a fuller and more accurate knowledge of the development of the cava in each individual form, but also a clearer understanding of the general developmental factors which influence and govern the establishment of the posterior vena cava in all mammals and an insight into the modiﬁcations in these factors which result in the differences in the formation of the cava among different species.

The work of Huntington and McClure (’20) enabled them to construct a composite diagram which included all the embryonic veins of the cat which make their appearance at one time or another during the course of ontogeny. Subsequent investigation has shown that the cat is particularly favorable for a study of venous development, for during the course of development in the cat there appear all of the principal venous channels which have been found in mammals. The composite diagram by Huntington and McClure is, therefore, of much wider application than was originally supposed; it is in reality a diagram not alone of the veins in the cat, but rather of the principal veins found in the embryos of all mammals investigated. Thus it may be termed a composite diagram of the embryonic veins of mammals, and it is here reproduced in ﬁgure 26. By means of this single diagram one may trace the course of venous development in each of the mammals studied during the course of this or any previous investigation and may understand the part played by each of the embryonic veins associated in the formation of the adult posterior vena cava. DEVELOPMENT or THE POSTERIOR VENA CAVA 343

We ﬁnd that the development of the prerenal division of the vena cava is virtually the same in all species of mammals. In every mammal thus far investigated this portion of the cava results from the establishment of the hepato-subcardinal junction and is made up in all cases of the same two primary embryonic subdivisions: a pars hepatica (P.Hep.) coming from the vena hepatica communis, the liver sinusoids, and an independent vein within the caval mesentery, and a pars subcardinalis (P.Snbe.), representing a portion of the right subcardinal vein. A similar uniformity of development does not characterize the postrenal division of the vena cava; among different species of mammals this portion of the cava exhibits great variation, and it is this dissimilarity in development which in the past has given rise to the varied accounts set forth by different investigators. In preceding pages the writer has shown that the differences in the formation of the vena cava among various species of mammals are essentially differences in the relative role played by the posterior cardinal and the supracardinal veins. In one mammal the postrenal division of the vena cava may be predominantly supracardinal in origin, in another it may be partly supracardinal and partly posterior cardinal, while in still another it may be entirely posterior cardinal. In the cat, man, pig, sheep, and bat, for example, the postrenal division of the adult cava (ﬁg. 26) comes from the right supracardinal vein (B) and the right subcardino—supracardinal anastomosis (Sabe.8pre.Anast.). (A portion of a subcardino-posterior cardinal anastomosis (Snbc.Pc.Anast.) is included in the vena cava of the cat, as shown in ﬁgure 26;~in the other mammals mentioned, the subcardino—supraeardinal anastomosis (Snbe. Sprc.Anast.) passes directly between the subcardinal and supracardinal veins.) In the rabbit the postrenal division of the vena cava is made up of a right subcardino-posterior cardinal anastomosis (Siabe.Po.Anast.), and below this of portions of both the right posterior cardinal vein (A) and the right supracardinal vein (B). In the rat the postrenal division of the vena cava comes entirely from the right posterior 344 ELMER G. BUTLER

cardinal vein (A), which is always situated medial rather than lateral to the ureter.

Not only does the role of the posterior cardinal and the supracardinal veins differ among mammals, but also the part which the subcardinal veins play during the course of development varies in the different species. In some cases, as in the pig and in man, lumbar posterior cardinal veins disappear at a relatively early stage as continuous longitudinal channels, and the venous drainage of the mesonephroi in the lumbar region is then transferred to the right and the left subcardinal veins, which consequently become large and important channels and retain their independence and individuality to a late stage of development. In the cat and in the bat, on the other hand, subcardinal veins as prominent vessels disappear early in the lumbar region, while the lumbar posterior cardinal veins persist till a relatively late stage and continue to serve as the chief drainage veins of the mesonephroi. In bat embryos the early disappearance of subcardinal veins is associated with the virtual absence of a ventral intersubcardinal anastomosis and the substitution for it functionally of a prominent dorsal intersupracardinal anastomosis, the dorsal side of the renal collar (ﬁg. 26), which persists throughout ontogeny and in the adult bat constitutes a part of the left renal vein. In the rat and in the rabbit, subcardinal Veins caudal to the intersubcardinal anastomosis never become particularly large and they disappear at a relatively early stage of development.

Evidently, there must be in the embryos of mammals some developmental factoriwhich governs the role of the embryonic veins and whose Variation underlies the typical and characteristic dissimilarities among different species of mammals in the development of the caval vein. This variable developmental factor appears to be the functional activity of the mesonephroi.‘ Anyone who studies venous development in mammals cannot fail to be impressed with the very close relationship between the developing venous system and the embryonic excretory organs. When we ﬁnd, therefore, that the DEVELOPMENT OF THE POSTERIOR VENA CAVA 345

activity of the mesonephroi Varies in a deﬁnite and character— istic fashion among different species of mammals, We are not surprised to discover that the development of the Venous system, in particular the vena cava, varies accordingly.



Posterior Car-din¢1(Pc.xl

Supracardinai (A zyg cs)

Cu-ud_n'lV-i . ' 2 6

Fig. 26 Composite anagram of the embryonic veins of mammals. From Hunt— ington and McClure (’20)., 346 ELMER G. BUTLER

On the basis of the functional activity of the mesonephros, mammals may be divided into three groups: ﬁrst, those in which the mesonephros is never functional, so far as has been determined; secondly, those in which the mesonephros is early functional, but in which its activity declines at a relatively early stage; thirdly, those in which the activity of the mesonephros increases steadily over a rather long period of embryonic development. To the ﬁrst group belongs the rat, in which mesonephric glomeruli, according to Bremer (’16), never develop. To the second group belongs the rabbit, in which the mesonephros reaches the peak of its functional activity at between 9 mm. and 14 mm., after which its activity gradually declines. In the third group we may place man, the pig, sheep, and cat. In human embryos Bremer shows that the mesonephros early develops to its full capacity, and, in contrast with the condition in the rabbit, retains its full functional activity to a relatively advanced stage; a 30-mm. human embryo, for example, has the same number of mesonephric glomeruli as one at 13 mm. The pig, sheep, and cat are all closely similar. The mesonephros is not equally large in all three, but the functional activity in each is maintained to a relatively very late stage; in the pig the mesonephros increases in activity up to the 40-mm. stage; in the sheep the same number of mesonephric glomeruli are present in an embryo of 40.4 mm. as in one of 15.8 mm.; in the cat mesonephric activity becomes steadily greater up to 32 mm. It is evident, therefore, that a classiﬁcation of mammals on the basis of mesonephric activity corresponds with their classiﬁcation as regards the embryonic composition of the vena cava. In embryos in which mesonephric activity persists over a rather long period (man, pig, sheep, and cat) we ﬁnd welldeveloped supracardinal veins which enter into the formation of the caval vein; where mesonephric activity is early arrested (rabbit), supracardinal veins are developed to a relatively slight degree, and where mesonephric activity is entirely absent (rat), supracardinal veins as such do not appear.“

1‘ To the writer ’s knowledge, no study of the functional activity of the meso nephros in bat embryos has ever been made. The bat cannot be included, therefore, in this classiﬁcation. DEVELOPMENT or THE POSTERIOR VENA (JAVA 347

The mesonephros exerts a direct effect on the embryonic posterior cardinal vein. As a result of the steady and rapid increase in mesonephric activity, in embryos of the pig and the sheep, the lumbar division of each posterior cardinal vein, after the formation of hepato~subcardinal junction, is broken up into a series of irregular veins on the dorsal surface of the mesonephros, which drain into the subcardinal vein; the same is true of the cardinal vein in human embryos (McClure and Butler, ’25, ﬁg. 15), although here the condition is somewhat less striking. In cat embryos, although each posterior cardinal vein in the lumbar region remains a continuous channel to a relatively late stage of development, it is, however, at all times very intimately associated with the mesonephros. Lumbar cardinal veins in the rabbit, on the other hand, follow a different course; instead of becoming increasingly more closely associated with the mesonephros, the cardinal vein separates from it rather early in development, namely, at about the 13-mm. stage. From this stage on, the lumbar cardinal vein of rabbit embryos, except in the region of the periureteric ring, is gradually divorced from the mesonephros as this is forced lateral under the influence of the migrating kidney. In older rabbit embryos only the portion of the cardinal vein (or its derivatives) which forms the lateral side of the periureteric ring remains as the main drainage vessel of the mesonephros. In the rat, as has been previously demonstrated, cardinal vein and mesonephros are never so closely associated as in other mammals. The principal function of the cardinal vein throughout development in the rat is the drainage of the dorsal body wall. As the migrating kidney in a rat embryo advances from'the level of the umbilical arteries, mesonephros and cardinal vein readily separate, allowing the kidney to pass between them. Therefore, the general course of development of the lumbar cardinal veins in pig, sheep, human, cat, rabbit, and rat embryos varies directly with the extent and the duration of mesonephric activity.

THE AMERICAN JOURNAL or ANATOMY, VOL. 39, NO. 2 348 ELMER G. BUTLER

Through their direct effect on the cardinal veins, the mesonephroi exert an indirect, but none the less important, inﬂuence on the development of the lumbar supracardinal veins. The origin and growth of lumbar supracardinal veins are due directly, according to the observations of the writer, to three principal developmental factors: the growth of the dorsal body wall, the migration of the kidneys, and the growth of the hind-limb buds. The operation of each of these three factors is in turn governed by the activity of the mesonephroi. In those mammals in which prominent supracardinal Veins develop and play an important role, as in the cat, man, pig, and sheep, it is found that they originate primarily in response to a demand for a drainage of the dorsal body wall more eﬁicient than that afforded by the posterior cardinal veins, which in these mammals are intimately, and in later stages, almost solely associated with mesonephric drainage. In rat embryos supracardinal veins as prominent longitudinal trunks never develop in the lumbar region, for the reason that lumbar posterior cardinal veins, owing to the absence of mesonephric activity, serve efficiently throughout development as the drainage vessels of the dorsal body wall. In rabbit embryos lumbar supracardinal veins develop only in the region of the small periureteric venous rings, for it is in this region alone that the main posterior cardinal channel remains in intimate association with the mesonephros; anterior to each periureteric ring the cardinal vein rather early in development separates from the mesonephros and throughout development continues to receive the dorsal somatic tributaries, with the result that in this region no supracardinal vein appears. The inﬂuence of the migrating kidney on the development of the supracardinals depends also to a great degree on mesonephric activity and its effect on the posterior cardinal veins. In all mammals investigated, except the rat, the migrating kidney passes medial to the cardinal vein, since this vein, or a portion of it, remains in contact with ‘the functionally active mesonephros, with the result that the kidney interferes, to some extent at least, with DEVELOPMENT or THE POSTERIOR VENA CAVA 349

the tributaries of the dorsal body wall, which up to this time have drained into the posterior cardinal vein or into the mesonephric tributaries on the dorsal surface of the mesonephros. This interference with the somatic tributaries in this region accelerates the development of the supracardinal veins. In the rat We ﬁnd that, since the kidney passes lateral, not medial, to the cardinal vein, there is virtually no disturbance of the tributaries of the lumbar posterior cardinal vein, and consequently no effect on the development of supracardinal channels. The immediate forerunner of right and left supracardinal veins is, in all cases, a ﬁne capillary plexus lateral and dorsal to the aorta, from which arise the longitudinal channels. Supracardinal veins When they ﬁrst appear are small capillary vessels. They owe their subsequent growth to the fact that the drainage of the hind-limb buds is soon transferred from the posterior cardinal veins or from the mesonephric circulation, as the case may be, to the supracardinal channels, which, therefore, increase rapidly in size and soon after their appearance become the largest veins in the lumbar region. In conclusion, therefore, it may be said that primarily it is the increasingly more intimate association of the lumbar posterior cardinal veins and the mesonephroi in the cat, man, pig, sheep, and bat which accounts for the development of prominent supracardinal veins in these mammals and the important part which they play in the development of the posterior vena cava; it is the decline in mesonephric activity and the release, so to speak, of the lumbar cardinal veins from the mesonephroi, except in the region of the periureterio ring, "which accounts for the very slight development of supracardinals in the rabbit, and that it is the lack of functional activity of the mesonephroi in the rat which leaves the cardinal veins free throughout development and consequently accounts for the absence of lumbar supracardinal veins.

On the basis of the present study of the comparative embryology of the mammalian posterior vena cava, we may conﬁdently expect that a study of still other mammals would 350 ELMER G. BUTLER

reveal only further differences in the relative role of the posterior cardinal, subcardinal, and supracardinal Veins. We may expect, furthermore, that were we able to modify experimentally, as may be possible in the future, the factors governing venous development, the resulting change in venous conﬁguration which might then occur would be essentially a change in the relative value of one or more of the embryonic channels. It is, undoubtedly, alteration in developmental factors Which underlies the origin of atypical or anomalous ve11ous conditions so frequently found in adult mammals.

SUMMARY

The posterior vena cava in the pig, sheep, and bat, as in the cat and in man, is composed of four embryonic subdivisions: pars hepatica from the vena hepatica communis, the liver sinusoids, and an independent vein within the caval mesentery; pars subcardinalis from a portion of the right subcardinal vein; pars renalis from an anastomosis between the right subcardinal vein and the right supracardinal vein; pars supracardinalis from the lumbar portion of the right supracardinal vein.

In rat embryos supracardinal veins as prominent longi— tudinal channels do not develop in the lumbar region of the body and the supracardinal system of Veins does not contribute, therefore, to the formation of the adult posterior vena cava. Lumbar posterior cardinal veins in the rat remain as continuous channels to a relatively late stage of development and a portion of the right posterior cardinal vein eventually forms the postrenal division of the posterior vena cava. In its entirety the posterior vcna cava of the rat is made up of three embryonic subdivisions: pars hepatica, pars subcardinalis, and pars cardinalis.

In the rabbit the prerenal division of the posterior vena cava is composed, as in other mammals, of a pars hepatica and a pars subcardinalis. The postrenal division is made up of a short anastomosis between the right subcardinal vein DEVELOPMENT 013‘ THE POSTERIOR VENA CAVA 351

and the right posterior cardinal vein and below this anas— tomosis of portions of both the right posterior cardinal and the right supracardinal veins. The dorsal half of the periureteric venous ring in the rabbit, which is homologous with the dorsal half of this ring in embryos of the cat, man, sheep, and bat, is considered as supracardinal in origin.

All differences observed in the development of the posterior vena cava are essentially differences in the relative functional role of the posterior cardinal, subcardinal, and supracardinal veins. The chief underlying cause for such differences is the dissimilarity among mammals in the size of the mesonephroi and particularly in the duration of their functional activity. In mammals in which the activity of the mesonephroi persists over a comparatively long period, as in the pig, sheep, cat, and man, the lumbar posterior cardinal veins (or their derivatives) are intimately and, in later stages, almost solely associated with mesonephric drainage; in these mammals prominent lumbar supracardinal veins develop, primarily in response to a demand for a drainage of the dorsal body Wall more etﬁcient than that afforded by the posterior cardinal veins, and eventually the right supracardinal vein enters directly into the formation of the postrenal division of the adult vena cava. In rat embryos supracar— dinal veins as prominent longitudinal trunks never develop in the lumbar region, chieﬂy because the lumbar posterior cardinal veins, owing to the absence of mesonephricactivity, serve efficiently throughout development as the drainage vessels of the dorsal body wall. In rabbit embryos,» where mesonephric activity declines rather early in development, lumbar supracardinal veins develop only in the region of the small periureteric venous rings, for it is in this region alone that the main posterior cardinal channel remains in intimate association with the mesonephros. 352 ELMER G. BUTLER

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