Paper - Development of the inferior vena cava (1929)

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Gladstone RJ. Development of the inferior vena cava in the light of recent research, with especial reference to certain abnormalities, and current descriptions of the ascending lumbar and azygos veins. (1929) J Anat. 64(1): 70-93. PMID 17104259

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This 1929 historic paper by Gladstone describes inferior vena cava development.



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Development of the Inferior Vena Cava in the Light of Recent Research

With especial reference to certain Abnormalities, and Current Descriptions of the Ascending Lumbar and Azygos Veins


By Reginald J. Gladstone, M.D., F.R.CS. University of London, King’s College

Introduction

Since the publication of Rathke’s, Kerschner’s and Hochstetter’s pioneer researches on the development of the venous system, a large amount of admirable work has been carried out on the development of the postrenal part of the inferior vena cava, both in animals and in man. The bulk of this work has been accomplished by American embryologists and more especially by Lewis, Miller, Huntington, McClure, Butler, Sabin and Reagan.


The older methods of reconstruction have now been supplemented by the intravascular injection of solutions of Indian ink, nitrate of silver, Prussian blue, and other dyes, into living embryos, the tissues being afterwards fixed, cleared and mounted in celloidin. This method has furnished most beautiful demonstrations of the finer vessels and their anastomoses, even in quite young embryos, e.g. rat embryos having only 2-3 somites (Reagan). But although, under ‘exceptional circumstances, the successful injection of a living human embryo has been accomplished (Broedel), the careful study and reconstruction of serial sections of human embryos is still the most valuable method of research with regard to the development of these blood vessels in man.

Comments On Current Descriptions Of The Ascending Lumbar And Azygos Veins

In three papers written before the publication of the more recent work of the above-mentioned authors, I recorded: (A) two cases of a dorsal position of the ureter relative to the inferior vena cava; (B) one of a postaortic course of the left renal vein; and (C) one of a left postrenal vena cava. In the article dealing with the postcaval position of the ureter, I drew attention to the development of the ascending lumbar vein, by the formation of a longitudinal anastomosis between the lumbar intersegmental veins. This vessel courses vertically in front of the transverse processes of the lumbar vertebrae, and behind the psoas major muscle (fig. 6 of that article).


The course of an anastomotic vein (text-fig. 1), which commonly arises from the dorsal aspect of the inferior vena cava, and proceeds upwards through the right crus of the diaphragm, or its aortic opening, to join the vena azygos major in front of the body of either the 12th or 11th thoracic vertebra, was also commented on, and figured. A similar anastomotic vein is frequently present on the left side, and passes into the thorax through the left crus of the diaphragm (text-fig. 1); this vein may arise from a left lumbar vein, the left renal vein or the inferior vena cava, and it usually joins the hemiazygos vein at the level of the body of the 12th thoracic vertebra.


Text-fig. 1. Drawing from an adult male subject showing the origin of the vena azygos major and vena azygos minor; and the relation of these vessels to the sympathetic chain, the splanchnic nerves, and the intersegmental arteries. The dotted lines indicate the position of the crura of the diaphragm.

ALV. Ascending lumbar vein. NSMi. Lesser splanchnic nerve. IA. Intercostal arteries. RLAzV. Right lumbar azygos vein. HAV. Hemiazygos vein. SC. Sympathetic cord. LLAzV. Left lumbar azygos vein. SCV. Subcostal vein.

NSMa. Greater splanchnic nerve.


The first accurate description of these anastomotic veins in the adult human subject, in this country, was by Robinson (22), who figured five cases, showing the origin of the right anastomotic vein, from the dorsal aspect of the inferior vena cava, at a point below the termination in it of the renal veins; and he also drew attention to the frequent termination of the Ist, and sometimes the 2nd lumbar vein in the anastomotic vein of the corresponding side. Unfortunately, however, although well aware of the relations, he did not in this paper make any allusion to the termination of the subcostal vein which unites, as is correctly described in the majority of textbooks on human anatomy, with the ascending lumbar vein. This union normally takes place behind the origin of the diaphragm, close to the head of the 12th rib, and by the side of the body of the 12th thoracic vertebra. On the right side the vein which is formed by the union of the subcostal vein with the ascending lumbar vein is regarded as the commencement of the vena azygos major, and the similar vein on the left side as the commencement of the vena azygos minor or hemiazygos vein. The subcostal vein passes into the thorax beneath the lateral lumbocostal arch; the ascending lumbar vein passes upward behind the psoas muscle, and beneath the medial lumbocostal arch. The vena azygos major then ascends in the thoracic cavity for a distance of one or two inches, before it is joined by the slender anastomotic vein (sometimes merely a fibrous cord, text-fig. 3), which ascends in front of the vertebral column either through the right crus of the diaphragm or its aortic opening. The statement therefore that the vena azygos major passes through the aortic opening of the diaphragm does not accord with the description of the origin of the vena azygos major, from the junction of the right subcostal vein, with the right ascending lumbar vein; and since the anastomotic vein in many cases does not pass through the aortic opening, but traverses the right crus of the diaphragm, and is sometimes represented only by an impervious cord, it is obvious that the alternative description of the vena azygos major arising in the abdomen from an “ascending lumbar vein” in front of the vertebral column and psoas muscle and passing through the aortic opening of the diaphragm is inconsistent with the more classical description of its origin in the thorax from the junction of the right subcostal vein with the ascending lumbar vein, namely, that vein which lies behind the psoas major muscle, and in front of the transverse processes of the lumbar vertebrae.

The necessity for a more exact description and drawings of the ascending lumbar veins, and of the origin of the vena azygos major, will be apparent on comparing the statements which are quoted below from current textbooks on human anatomy: ,

(1) The vena azygos major or right azygos vein commences in the abdomen, as the right ascending lumbar vein, and enters the thorax through the aortic opening of the diaphragm, lying on the right side of the aorta, the thoracic duct intervening. The ascending lumbar vein is depicted in a figure on the succeeding page as passing upward in front of the psoas muscle, although it is correctly described in the text under the heading of the Lumbar Veins: The vessels of each side are connected by a series of longitudinal anastomosing veins, in front of the lumbar transverse processes, and the longitudinal vessel thus formed is called the ascending lumbar vein.

(2) The azygos vein (O.T. vena azygos major) usually takes origin in the right ascending lumbar vein. It will be found in the interval between the right crus of the diaphragm and the aorta, upon the right side of the cisterna chyli, and it will be noticed to enter the thorax by passing through the aortic opening....The vena azygos commences in the abdomen where it anastomoses either with one of the upper lumbar veins or directly with the inferior vena cava.

(3) Between the crura and to the right of the aorta lies the right ascending lumbar vein, a longitudinal trunk linking together the transversely coursing lumbar veins, which pass inwards from under cover of the fibrous arches of the psoas to open into the inferior vena cava. This ascending lumbar vein is the beginning of the vena azygos major, but the latter vessel always has a communication with the back of the inferior vena cava as well. In many cases the ascending lumbar vein is hardly visible, and then the vena azygos rises entirely from the inferior vena cava.

(4) The larger or right azygos vein commences opposite the first or second lumbar vertebra, by a branch from the right lumbar veins (the ascending lumbar) ; sometimes by a branch from the right renal vein, or from the inferior vena cava. It enters the thorax through the aortic opening of the diaphragm.

(5) The vena azygos major begins in the abdomen, where it may be looked upon as the continuation upwards of the ascending lumbar vein. It passes through the aortic opening of the diaphragm....The trunk lumbar veins are connected beneath the psoas muscle by vertical branches, which cross in front of the transverse processes.

I would suggest that the term “ascending lumbar vein” be limited to the vertical precostal anastomosis, which extends between the iliolumbar vein and the termination of the subcostal vein; in other words, the longitudinal vessel behind the psoas major muscle which commences below in the iliolumbar tributary of the common iliac vein, and terminates above by uniting with the subcostal vein, to form on the right side the vena azygos major, and on the left side the vena azygos minor or hemiazygos vein.

I would also suggest that the small anastomotic vein which commences on the dorsal aspect of the inferior vena cava or from one of its tributaries near the termination of the right renal vein, and passes upward through the aortic opening of the diaphragm to join the vena azygos major, be called the right lumbar azygos vein; further that the classical description of the origin of the vena azygos major, by the union of the right ascending lumbar vein with the right subcostal vein, be retained, and as a corollary to this, that the description of the vena azygos major commencing in the abdomen as a continuation of the ascending lumbar vein and entering the thorax through the aortic opening of the diaphragm be discarded altogether.

Moreover, I would suggest that the corresponding vein on the left side, which passes upward in front of the vertebral column, and through the left crus of the diaphragm, be termed the left lumbar azygos vein, since both in the embryo and in the adult it has similar relations to those of the right side, with the exception that it usually arises from the dorsal aspect of the left renal vein (intersubcardinal anastomosis), or one of its tributaries, instead of directly from the inferior vena cava. Moreover, the vena azygos minor might be appropriately defined as arising by the junction of the left ascending lumbar vein with the left subcostal vein, and receiving as a tributary a short distance above its origin the small left lumbar azygos vein.

The employment of the terms “azygos” (without a yoke) and “hemiazygos” (half unyoked) is obviously incorrect. These names, however, have become so ingrained by long usage, that although from the academic standpoint it would be advantageous to replace them by a better term, from the practical standpoint it would be difficult to discontinue these old-established and familiar terms.

In addition to the use of the term “lumbar azygos veins” for the veins in the lumbar region, which are homologous with and continuous with the thoracic azygos veins, it will be necessary to explain the following terms which are applied by various authors to certain embryonic veins in this region: (1) Thoraco-lumbar veins described by Hochstetter and later defined by Reagan. These lie ventrolateral to the sympathetic chain and the nerves passing from the ganglionated chain to the preaortic plexuses; for a brief period these veins receive the segmental drainage which has been abandoned by the posterior cardinal veins; at a later stage of development they are succeeded by the medial parasympathetic veins, or permanent azygos system. (2) Medial parasympathetic veins (Reagan). These are in the azygos line and are used as synonyms for the azygos veins in the lower thoracic and lumbar regions. They lie medial to the sympathetic chain, dorsomedial to the nerves passing from the chain to the preaortic plexuses, and ventrolateral to the thoracic and lumbar intersegmental branches of the aorta. (8) Periganglionic plexus of veins (Frazer); “a plexus of veins formed around the groups of sympathetic ganglion cells as these pass out from the posterior root ganglia.”’ It joins laterally with the intersegmental veins, ventrally with the postcardinal and subcardinal veins, and it extends forwards to form a preaortic plexus, from which the intersubcardinal anastomosis is derived. It is also carried down into the pelvis dorsal to the umbilical arteries, and here appears to give rise to the common iliac veins, by an anastomosis in front of the caudal aorta (middle sacral artery) similar to the preaortic anastomosis which forms the terminal part of the left renal vein. He suggests also that the seeming continuity of the postcardinal veins with the pelvic vessels is due to these being derived originally from a continuation of the periganglionic plexus into this region. (4) The thoracic and lumbar supracardinal veins. These are described by Huntington and McClure as well defined, bilateral veins which are situated in the azygos lines. They are formed in the embryos of many mammals as well as in man, one on each side of the aorta, and are united more especially in the lumbar region by numerous postaortic anastomoses; the postrenal section of the vena cava was originally described as arising from the fusion of the right and left supracardinal veins, by enlargement of these anastomoses and disappearance of the spaces between them. In the human subject they succeed and replace the temporary thoraco-lumbar veins in the lower thoracic and upper lumbar regions, where they give rise to the “azygos” veins. In the lower lumbar region the right supracardinal vein gives rise to the inferior vena cava below the level of the renal veins. This part of the right supracardinal vein corresponds to the right paraureteric vein of Reagan, and a part of the postrenal section of the periganglionic plexus of Frazer. (5) Prevertebral plexus of Sabin, a general term for the veins lying in front of the vertebral column, which give rise to the azygos veins and postrenal vena cava. (6) Subcentral veins which differ from the azygos veins in lying dorsomedial to the origins of the intercostal and lumbar arteries, or in other words between the origins of these vessels. (7) The postrenal anastomosis or posteromedial limb of the venous ring which encircles the metanephros (Hochstetter). (8) Paraureteric vein (Reagan). This vessel lies medial to the kidney and ureter, and ventrolateral to the nerves, passing from the sympathetic chain to the preaortic plexuses.

The lumbar azygos veins, Plate II, figs. 2 and 4, like the lower part of the thoracic azygos veins, Plate II, fig. 1, lie medial to the sympathetic trunks ; dorsomedial to the splanchic nerves, text-fig. 1, and the nerves passing from the sympathetic chain to the preaortic and hypogastric plexuses, and they are situated ventrolateral to the origins of the lumbar segmental arteries. These relations of the azygos line of veins to the sympathetic nerves are well known, but the credit of appreciating the importance of their topographical relations in the study of the development of the inferior vena cava is entirely due to Dr F. T. Reagan. The significance of their position with regard to the preaortic plexuses and lumbar arteries will be referred to later.

DESCRIPTIONS OF ABNORMAL INFERIOR VENAE CAVAE

Specimen 1 (text-fig. 2). This is a typical example of the arrangement of veins in this class of anomaly, namely, bilateral postrenal vena cava. The left inferior vena cava commenced in front of the body of the 5th lumbar vertebra, from the left common iliac vein, which vessel, having given origin to the left inferior vena cava, passed obliquely upward behind the origin of the right common iliac artery, to join with the right common iliac vein in forming the right inferior vena cava. The left vena cava coursed vertically upward beside the aorta to the level of the termination in itself of a lower left renal vein. It then turned to the right and crossed the aorta below the origin of the superior mesenteric artery; finally it joined the right vena cava in front of the origin of the right renal artery. This terminal part of the left inferior vena cava received an upper left renal vein, and a venous trunk formed by the union of the left suprarenal vein with the left inferior phrenic vein. The left spermatic vein joined the lower left renal vein. The left ascending lumbar vein commenced as an upward continuation of the lumbar tributary of the left iliolumbar vein, which vessel opened below into the left common iliac vein. The left ascending lumbar vein passed upward behind the psoas major-muscle, and finally ended in the upper of the two left renal veins. It received the 5th, 4th and 3rd left lumbar veins, the 3rd and 4th being continued medially from the ascending lumbar vein into the left inferior vena cava. Nearly opposite the termination of the ascending lumbar vein in the left renal vein, a vein (which represents the left anastomotic or lumbar azygos vein) passed upwards behind the principal left renal artery and two accessory renal arteries, towards the vertebral end of the 12th rib, below which it divided into two branches; the lateral of these joined the subcostal vein, and the medial joined the common trunk formed by the union of the lateral branch with the subcostal vein in front of the head of the last rib.



Text-fig. 2 (Specimen 1). Bilateral postrenal vena cava. Note the termination of the right lumbar azygos vein in the vena azygos major at the level of the 12th thoracic vertebra, and its origin from the dorsal aspect of the inferior vena cava below the entrance of the renal veins;. also the origin of the left lumbar azygos vein, in common with the upper left renal vein from a corresponding position on the other side. The ascending lumbar veins which lie close to the vertebral column, and behind the psoas muscles and inferior venae cavae, have been represented in the drawing more lateral than their true position.

AHY. Accessory hemiazygos vein. LLAzV. Left lumbar azygos vein. ALY. Ascending lumbar vein. ISI. Left superior intercostal vein. HAZY. Hemiazygos vein. RLAzV. Right lumbar azygos vein. IPhV. Left inferior phrenic vein. RSI. Right superior intercostal vein. ILV. Tliolumbar vein. SCV. Subcostal vein.

ISY. Internal spermatic vein. VAMa. Vena azygos major.

L. 1, 2,3, 4. Lumbar intersegmental veins.

The right inferior vena cava was formed in the usual way by the junction of the right and left common iliac veins, and from thence upward it pursued the ordinary course of the inferior vena cava on the right of the aorta. It may be noted that this case supports the statement made by Cameron that the right iliolumbar vein joins the common iliac vein at a higher level than the termination of the left iliolumbar vein in the left common iliac vein; and also that on neither side was there a direct communication with or termination of the 5th lumbar vein in the inferior vena cava. Owing to this relation, Cameron conceived the terminal part of the left common iliac vein (interiliac anastomosis) as representing in the adult the enlarged terminal segment of the left 5th lumbar vein. The right ascending lumbar vein had similar relations to those of the left ascending lumbar vein. It passed upward behind the psoas muscle, and terminated above by passing beneath the medial costolumbar ligament, joining the right subcostal vein in front of the head of the last rib. An anastomotic or right lumbar azygos vein commenced from the posterior aspect of the inferior vena cava below the entry of the right renal vein, passed upward through the right crus of the diaphragm, and joined the azygos vein at the level of the 12th thoracic vertebra.

There were two right spermatic veins. One of these joined the right inferior vena cava at the level of the 3rd lumbar vertebra, the other terminated at the angle of junction of the left with the right inferior vena cava.

In the thorax the hemiazygos vein crossed the body of the 9th thoracic vertebra; the accessory hemiazygos that of the 8th.

Specimen 2 (text-fig. 8). Bilateral postrenal vena cava. A complete description of all the vessels is unnecessary, since the general arrangement of the veins is indicated in the drawing. The middle sacral vein divided into right and left branches, each of which joined the corresponding postrenal segment of the inferior vena cava. The anastomotic or lumbar azygos vein of the right side appeared to arise from the Ist lumbar vein. The terminal part of this vein, however, which runs obliquely downwards to join the vena cava, probably represents the primary origin of the anastomotic vein from the dorsal aspect of the inferior vena cava, close to the termination of the right renal vein. It received a communicating branch from the right ascending lumbar vein, namely, a part of the first lumbar segmental vein. On tracing the anastomotic vein upward it became reduced to a fibrous cord, which traversed the right crus of the diaphragm, and finally becoming pervious in its upper part ended in the vena azygos major, in front of the 12th thoracic vertebra.

The left anastomotic or lumbar azygos vein commenced in a similar manner from a common trunk, which received the Ist and 2nd left lumbar veins. This trunk vein terminated below in the left inferior vena cava, at the level of the entrance into it of the left renal vein. On tracing the anastomotic vein upward it was found to terminate in a fibrous cord, which traversed the left crus of the diaphragm and, finally becoming pervious, joined the vena azygos minor.

Specimen 8 (text-fig. 4) is an example of the formation of the inferior vena cava, in front of the right common iliac artery. It occurred in a male subject. The middle sacral vein, near its termination, divided into right and left branches, which ended one on each side in the corresponding common iliac vein. The right common iliac vein was joined on its posterior aspect by two veins; one an iliolumbar vein, the lumbar branch of which was continuous above with the ascending lumbar vein, the other a descending lumbar vein which received tributaries from the psoas muscle and spinal canal. On the left side the common iliac vein received a separate iliac vein and a normal iliolumbar vein which was continuous by means of its lumbar branch with the ascending lumbar vein of the same side. A large right internal spermatic vein joined the inferior vena cava at a level corresponding with the origin of the inferior mesenteric artery from the abdominal aorta.



Text-fig. 3 (Specimen 2). Bilateral postrenal vena cava. The central part of each lumbar azygos vein is reduced to a fibrous cord. Above, each fibrous cord becomes patent and joins the thoracic azygos vein of the corresponding side. Below, the right lumbar azygos vein after being joined by the first and second lumbar veins terminates in the inferior vena cava. The left lumbar azygos vein ends below in a similar manner, after having been joined by the upper lumbar veins of the left side. It terminates on the dorsal surface of the left inferior vena cava where this is joined by the left renal vein.

ALV. Ascending lumbar vein. LSIV. Left superior intercostal vein. HAzV. Hemiazygos vein. RLAzV. Right lumbar azygos vein. IPhV. Inferior phrenic vein. RSIV. Right superior intercostal vein. ILV. Tliolumbar vein. SCY. Subcostal vein.

ISV. Internal spermatic veins. VAMa. Vena azygos major.

LV. Lumbar intersegmental veins. VSM. Vena sacralis media.

LLAzV. Left lumbar azygos vein.

Specimen 4 (text-fig. 5). The most noticeable peculiarities of this case are: (1) The very large size of the inferior vena cava. (2) The presence of a large vein on the left side of the abdominal aorta, which commenced in a plexus of dilated veins situated in the broad ligament of the uterus; it ascended in front of the internal iliac vessels and ureter, then passed upwards on the psoas major muscle, lateral to the sympathetic chain and in front of the left ovarian artery; just below the level of the origin of the inferior mesenteric artery it received the left ovarian vein, which joined it obliquely from the outer side; near the upper pole of the left kidney it was joined by the left renal vein; the common trunk thus formed crossed the abdominal aorta below the origin of the superior mesenteric artery, and then terminated in the inferior vena cava; this common trunk received (A) a superior polar vein from the left kidney which passed behind the suprarenal body, (B) the left suprarenal vein, and (C) the left inferior phrenic vein. The left kidney was unusually low in position and the left renal vessels were thus obliquely placed and much elongated. (3) The right ovarian vein received an accessory inferior polar vein from


Text-fig. 4 (Specimen 3). Origin of the inferior vena cava ventral to the right common iliac artery.

AL. Ascending lumbar vein. IVC. Inferior vena cava.

AMI. Inferior mesenteric artery. LV. Lumbar vein.

ILV. Iliolumbar vein. RIS. Right internal spermatic vein. IV. Iliac vein. VSM. Middle sacral vein.

the kidney of the corresponding side; this vessel received a tributary which ascended from the retroperitoneal fatty tissue below the kidney, and crossed in front of the right ureter. (4) An accessory renal artery arose from the ventral aspect of the abdominal aorta just above its bifurcation, and ascended obliquely over the inferior vena cava, to reach the hilum of the right kidney. It was crossed superficially by the ovarian vessels and the pelvis of the ureter.

Specimen 5. In this case the inferior vena cava was normal in position, but was joined by a large vein from the left side, which passed behind the abdominal aorta at the level of the origin of the inferior mesenteric artery. This vein commenced near the hilum of the kidney from the lower border of the left renal vein. It was joined here from below by a short common trunk formed by the union of two left ovarian veins. It was joined from above by a tributary which descended in the retroperitoneal fatty tissue, and from below by the 8rd left lumbar vein. It was also joined from below, near its termination, by a prevertebral or subcentral vein, which ran upwards to it behind the abdominal aorta. The 4th left lumbar vein crossed behind the aorta about 2 cm. below the large postaortic tributary from the left renal vein. The main left renal vein crossed in front of the aorta in the usual position below the origin of the superior mesenteric artery. The right ovarian vein ended in the inferior vena cava in the usual manner a short distance below the termination -of the right renal vein.


Text-fig. 5 (Specimen 4). Persistence of left subcardinal vein. Accessory renal veins and accessory renal artery. The large vein on the left side of the abdominal aorta commenced in a plexus between the layers of the broad ligament, crossed in front of the iliac vessels, the ureter and left ovarian artery and terminated in the left renal vein.

AcRA. Accessory renal artery. LOvV. Left ovarian vein. AcRV. Accessory renal veins. LSV. Persistent left subcardinal vein. IPhV. Inferior phrenic vein. ROvV. Right ovarian vein.

There were two ovarian arteries on the right side, one springing from the front of the aorta below the left renal vein, crossed behind the inferior vena cava, the other arose from the aorta below the origin of the inferior mesenteric artery, crossed obliquely over the lower part of the inferior vena cava, and joined the former vessel below the level of the bifurcation of the aorta. An excellent drawing of this specimen by Francis W. Kemp is contained in the Record of Anatomical Variations, King’s College, London, 1915.


Review of the Developmental History of the Inferior Vena Cava

The explanation of these anomalies will be facilitated by a review of the normal development of the inferior vena cava in man, and this will help to substantiate further the comments which I have made earlier in this paper regarding the ascending lumbar and azygos veins. Such a revision of recent work is of especial importance at the present time, since although there is full agreement on the mode of development of the inferior vena cava in its earlier stages, there are fundamental differences of opinion with regard to the later stages. Taking into consideration the important pioneer work of the authors cited in the appended list of references which forms the foundation of our knowledge of this subject, and with the help more particularly of the recent work of McClure and Butler in the human subject; of Reagan and Tribe in the rabbit, and of Reagan and Robinson in man and the carnivora, I venture to give the following brief summary of what I believe to be the main features of the development of the inferior vena cava and azygos system of veins in man.

Commencing with the bilaterally symmetrical venous system of a 4mm. human embryo (McClure and Butler), it is seen that at this stage there are two large posterior cardinal veins which commence in the caudal region and terminate cranially by joining with the anterior cardinal veins to form the ducts of Cuvier. They receive visceral tributaries from the Wolffian bodies and somatic intersegmental veins from the body wall and spinal cord. They are also connected by anastomoses with the two small subcardinal veins which lie in the mesonephros near the root of the mesentery. Each subcardinal vein ends anteriorly in the posterior cardinal vein of the corresponding side. The posterior cardinal veins lie dorsolateral to the umbilical arteries, and extend a considerable distance in the caudal region beyond these, and the caudal ends of the mesonephroi. The part of each posterior cardinal vein which extends beyond the mesonephros, and receives tributaries from the body wall, may be distinguished as the pelvic segment, and its drainage is mainly somatic. That part of each posterior cardinal vein which receives tributaries from the mesonephros, as well as from the body wall and spinal cord, is the mesonephric segment, and the part which extends headward from the termination in it of the anterior end of the subcardinal vein to the duct of Cuvier may be distinguished as the terminal thoracic segment.

In the 10-11 mm. stage represented by the reconstruction models of McClure and Butler, the two subcardinal veins are connected across the front of the abdominal aorta by a plexus of veins, the preaortic intersubcardinal anastomosis. This lies below or caudal to the origin of the superior mesenteric artery. The primary connection of the anterior ends of the subcardinal veins with the posterior cardinal veins has now been interrupted. Further, the important connection of the right subcardinal vein with the hepatic sinuses and the common hepatic vein is already established, as is also the interiliac anastomosis between the posterior cardinal veins. This anastomosis is situated below the bifurcation of the abdominal aorta, and between the umbilical arteries (which curve forward ventral to it) and the middle sacral artery which lies dorsal to it. The terminal part of the left common iliac vein is thus already laid down and in McClure and Butler’s reconstruction of a 10-11 mm. embryo, and in four of my own specimens (9, 10, 11 and 12 mm. in length), the succeeding part of the right posterior cardinal vein is considerably larger than the corresponding part of the left posterior cardinal vein. Moreover, this part of the postcardinal vein is displaced in a dorsolateral direction, by the growth of the permanent kidney; the posterior cardinal vein thus forms a C-shaped bend round the outer border of the kidney, the umbilical artery intervenes between the vein and kidney. Ventral to the metanephros and medial to the umbilical artery on each side is the caudal end of the subcardinal vein and the vein which drains the caudal end of the mesonephros. This may be regarded as the terminal part of the mesonephric segment of the posterior cardinal vein. In younger embryos the caudal ends of the subcardinal and caudal mesonephrie vein are connected by a terminal anastomosis. Later this connection is interrupted and the two veins commence separately.

Below the junction of the caudal mesonephric vein with the main posterior cardinal vein, a vein passes upward on each side from the interiliac anastomosis, in front of the umbilical artery, and joins the pelvic or somatic part of the postcardinal vein. This is the ventral limb of the circum-umbilical venous ring, which on each side surrounds the future common iliac artery. It has probably persisted in Specimen 3, text-fig. 4, and taken the place of the dorsal limb which is formed by that part of the posterior cardinal vein which drains the caudal end of the embryo.

A reference to Plate I, fig. 4, shows that in a 12 mm. human embryo in the region which corresponds to the caudal end of the mesonephros, the primary somatic tributaries of the posterior cardinal are being transferred to a postrenal anastomosis, and in the region of the suprarenal body, Plate I, fig. 8, and at the cranial end of the mesonephros, Plate I, fig. 2, a similar transference to a more dorsally situated vein has taken place; the somatic intersegmental veins, which primarily opened directly into the postcardinal veins, now terminate in a longitudinal vein which ends in the posterior cardinal vein at the level of the 6th thoracic vertebra. The cranial end of the mesonephros and that part of the posterior cardinal vein which is contained within it soon degenerates, and the primary continuity of the upper mesonephric segment of the posterior cardinal vein is interrupted. A similar degenerative change takes place at the lower end of the mesonephros, the transverse lumbar intersegmental veins now draining into the postrenal anastomosis, which soon becomes connected by an anastomotic vein with the subcardinal vein of the corresponding side, above the level of the metanephros. The postrenal anastomosis obviously corresponds to the anastomosis behind the kidney, first described by Hochstetter in the rabbit, which is formed by the union of the 16th with the 17th and 18th “thoracolumbar veins.”’ It lies dorsomedial to the kidney, and below the level of the intersubcardinal anastomosis. Further, it forms with the adjoining part of the posterior cardinal vein, which lies ventrolateral to the kidney, the perinephric venous ring of Hochstetter!. The dorsal limb of the perinephric ring is ventrolateral to the sympathetic nerves passing from the sympathetic chain to the preaortic and hypogastric plexuses, and these nerves pass between it and the aorta. Its position relative to these nerves therefore is that of the permanent inferior vena cava, Plate II, fig. 2. In a 19mm. human embryo the continuity of the ventrolateral limb of the periureteric ring has become interrupted, the posterior cardinal vein in this situation having completely disappeared. The dorsomedial limb, the inferior vena cava, has on the other hand become greatly enlarged, especially on the right side. It now receives tributaries joining it on the ventral aspect from the venous plexus in front of the aorta, Plate II, fig. 2. This preaortic venous plexus receives veins coming from the mesonephros and genital gland which lie in front of or ventromedial to the ureter, and communicates also with the subcardinal veins. The postrenal vena cava on each side also receives two series of tributaries on the dorsal aspect, (1) intersegmental veins situated ventrolaterally to the sympathetic chain and rami communicantes and (2) intersegmental veins which lie dorsomedial to the sympathetic chain. The latter are joined by a discontinuous longitudinal intersegmental vein, the lumbar azygos vein, Plate II, fig. 2, which lies medial to the sympathetic chain, and ventrolateral to the lumbar arteries. The lumbar veins are also connected at this stage of development by a newly-formed longitudinal vein which is situated in front of the transverse processes of the lumbar vertebrae and behind the psoas muscle. This is the ascending lumbar vein. It is continuous above with a vein similarly situated in the thoracic region (Plate II, fig. 1). In the thoracic region at this stage longitudinal thoraco-lumbar veins which are present in an 11 mm. embryo, Plate I, fig. 1, have been replaced (19 mm. human embryo) by the permanent thoracic azygos veins, which are situated medial to the sympathetic trunk, and dorsomedial to the splanchnic nerves. In the lower thoracic region and upper part of the lumbar region the azygos veins appear to be compressed by the crura of the diaphragm and the upward current of the blood interfered with. A new channel is thus formed for the blood coming from the upper intersegmental veins in the lumbar region, by the enlargement of the corresponding part of the ascending lumbar vein; this joins the subcostal vein on each side, under cover of the medial

1 Hochstetter describes in the rabbit a later stage in which the “perinephric” ring is succeeded by a “periureteric” ring. In the human subject and in the cat (Hochstetter), in the mole (Zumstein) and in the Mikrochiroptera (Grosser) the collateral vein lies primarily dorsomedial to the metanephros.

In the guinea-pig the “island formation” around the kidney does not take place, and in this type the metanephros migrates headwards on the ventral aspect of the posterior cardinal vein, and in Hrinaceus Huropaeus the ventral limb of the island frequently persists throughout life, lumbocostal arch, which protects the vein from pressure. The lumbar azygos vein in this region does not as a rule entirely disappear, but persists as the small anastomotic vein which on the right side joins the dorsal aspect of the inferior vena cava, or one of its lumbar tributaries; and on the left side joins the left renal vein or a left lumbar vein. If the lumbar azygos vein becomes completely obliterated in the region of the crura of the diaphragm, the current of blood will be reversed in the lower part of the vein and flow downwards into the inferior vena cava, or on the left side into the left renal vein. Below the level of the second lumbar vertebra the lumbar azygos veins in the human embryo are not developed to the same extent as in the thoracic region, and do not as a rule form a perfectly continuous channel. Reagan and Strong have shown that they take part with the subcentral or prevertebral veins in the formation of the terminal parts of the definitive left lumbar veins. The veins of the left side being carried across the front of the vertebral column behind the aorta by anastomoses formed between the subcentral veins, a pair of longitudinal vessels, which appear about the 45 mm. stage (earlier in my specimens) and lie between the origins of the lumbar arteries. The subcentral veins thus serve as a link between the lumbar azygos veins. Reagan has also pointed out that the lumbar azygos veins are formed independently of the tight and left inferior venae cavae (medial paraureteric veins) and that the azygos line is separated from the vena caval line by the branches of the sympathetic nerves, which pass from the sympathetic chain to the preaortic plexuses. The connection of the lumbar continuations of the thoracic azygos veins with the postrenal caval veins thus appears to be a secondary one. Moreover, it is evident that if the inferior vena cava is primarily developed in the azygos line, these nerves would pass both in the embryo and in the adult, superficial or ventrolateral to the inferior vena cava, instead of between this vessel and the abdominal aorta. It will be necessary here to allude to the development of the thoracolumbar veins, Plate I, fig. 1. The term “‘thoracolumbar” has apparently been used by some of the earlier authors to designate different vessels. Recently, however, the thoracolumbar lines have been defined by Reagan and Tribe, who describe in the rabbit a transitory pair of longitudinal veins, which arise from a plexus of capillaries situated lateral to the aorta. They extend from the midthoracic level to the sacral region. In the caudal half of the thorax these vessels are named the thoracolumbar veins. They receive the intersegmental veins, which originally drained into the mesonephric segments of the posterior cardinal veins, and convey the blood caudally into the transverse element of the inferior vena cava (‘‘renal collar” of Huntington and McClure). They serve as temporary substitutes for the adjoining parts of the posterior cardinal veins, while these are degenerating and until the establishment of the azygos veins. For a short period the thoracolumbar and azygos veins coexist. When the azygos vessels have become functional, and once more carry the blood headward to the superior vena cava, the thoracolumbar veins disappear. Similar vessels appear to be present in human embryos, which are of a temporary nature, and are functional between the 10 and 15 mm. stages, Plate I, fig. 1.


The lumbar segments of the longitudinal thoracolumbar lines of veins are distinguished by Reagan and Robinson as the “ paraureteric veins.” For a time they are symmetrical; the right, however, soon enlarges and persists as a part of the postrenal vena cava. The left eventually disappears. In the lumbar region the intersegmental veins which originally opened into the posterior cardinal veins are transferred to the paraureteric veins (or the corresponding parts of the right and left inferior venae cavae). The relation of the intersegmental tributaries of the paraureteric veins to the sympathetic trunk is a double one. Primarily they lie lateral to the sympathetic trunk and enter the paraureteric vein directly; later they pass dorsomedial to the sympathetic cord, enter the medial sympathetic vein (lumbar azygos) and by transverse communications of this with the paraureteric vein terminate indirectly in this vessel (namely, the inferior vena cava), Plate II, figs. 2, 3, 4.

A careful consideration of the different descriptions of the development of the inferior vena cava leads to the conclusion that the discrepancies are not so great as they appear, and that the account of the development of the postrenal segment of the vena cava has been rendered more difficult by. different names having been applied to the same venous channels. This difficulty could be removed to a certain extent if the term inferior vena cava be applied to the main venous channel in the embryo, as soon as the definitive ‘course is established, and the embryonic terms only used as adjectives to ‘indicate the vessel from which a particular part of the vena cava has been derived.

An examination of a series of human embryos in my possession, ranging from 9 to 65 mm. in length, shows that large parts of the posterior cardinal and subcardinal veins degenerate completely and are replaced by a laterformed longitudinal vein or veins, and also that when once the dorsomedial limb of the periureteric ring is completed, and the anastomosis of this collateral channel with the right subcardinal is established, the main venous channel, the inferior vena cava, persists, though its position and relations become somewhat altered. It becomes more medial, and as it does so, the terminal parts of the lumbar intersegmental veins, which primarily passed ventrolateral to the sympathetic trunk, are replaced by lumbar veins the terminations of which pass dorsomedial to the sympathetic trunk. The latter veins primarily open into the lumbar azygos veins; later, by means of secondary communications of the azygos vein with the inferior vena cava, they drain permanently into the vena cava. Still later the lumbar azygos vein itself appears to become incorporated in the main channel, the inferior vena cava not being replaced by a vessel in the azygos line, but the lumbar azygos vein becoming absorbed into it, by the widening out and shortening of the communicating branches between the two longitudinal vessels, Plate II, fig. 4.

Above the level of the entrance of the two definitive renal veins into the inferior vena cava, the right lumbar azygos vein persists as the vessel which in the adult connects the inferior vena cava with the right thoracic azygos vein, or vena azygos major. In this situation incorporation of the azygos vein into the inferior vena cava cannot take place on account of the vena cava being carried forward, and separated from the azygos vein by the right crus of the diaphragm.

Late embryos (22 mm. in length and older) show postaortic anastomoses between the right and left inferior venae cavae (supracardinal veins of Huntington and McClure) by which blood can be drawn off from the smaller left vena cava into the larger right vena cava, and the size of the left still further diminished, but there is no indication of a complete longitudinal fusion of these two vessels, like that of the right and left dorsal aortae. This possibility is negatived by the position between them of the paired origins of the lumbar intersegmental arteries (Reagan). This position of the lumbar arteries in an adult animal is exemplified by the Australian Duck Bill (Ornithorhynchus paradozus). A dissection of the abdominal vessels from an adult specimen of this primitive mammal, which is figured by Hochstetter, shows the lumbar arteries passing backwards in this position between the right and left inferior venae cavae; the latter are of approximately equal size, and lie close together one on each side of the abdominal aorta, and also on each side of the origins of the lumbar intersegmental arteries. If in such an animal a direct fusion were to take place in the intervals between the lumbar arteries, then these vessels would necessarily pass right through the inferior vena cava. It is obvious that this direct fusion of the right and left inferior venae cavae does not take place n the human embryo, in which the two venae cavae are separated by a considerable interval, and a flattened remnant of the left inferior vena cava is seen for a period of two or three weeks on the left side of the aorta. In those animals in which the left inferior vena cava persists until a relatively late period of foetal life, the ultimate disappearance of the left vessel appears to be, not by direct fusion of the two veins, but by means of the anastomoses of postaortic or prevertebral tributaries, which by enlargement form wide transverse communications in the intervals between the origins of the paired lumbar arteries. The blood is thus drawn off from the left into the right vena cava, the latter vessel forming a more direct route to the heart than the left. The left vena cava consequently diminishes still further in size, and eventually its continuity opposite, and to the left of the origins of the lumbar arteries, is broken and the vein finally disappears.

Obviously that part of the inferior vena cava, which is described by Reagan as derived from the “paraureteric” vein, corresponds to the part which originates from the lumbar segment of the “supracardinal” vein of Huntington and McClure. The lumbar supracardinal veins are, however, described by the latter authors as morphologically continuous with the thoracic supracardinal veins, these latter veins being in the true azygos line, and giving rise in the human subject on the right side to a part of the vena azygos major, and on the left side to the corresponding part of the vena azygos minor. The origin of the communicating vein (right lumbar azygos) from the posterior aspect of the inferior vena cava, and its continuity above with the thoracic azygos vein in the adult human subject, is evidence in favour of this conclusion. On the other hand, the “paraureteric” vein and the part of the inferior vena cava which is derived from it, lies ventrolateral to the nerves passing forward from the sympathetic chain to the preaortic plexuses, and thus occupies the ‘“‘thoracolumbar line” and not the true “azygos line.” If, however, the lower or caudal part of the lumbar azygos vein becomes incorporated in the inferior vena cava in the way suggested, this difficulty with regard to the relationship of the nerves is overcome. The inferior vena cava, which, when its course is first established, lies in the thoracolumbar line (paraureteric), incorporates or absorbs into itself the incompletely developed, often discontinuous lower part of the lumbar azygos vein, so that the main vessel in this region, from about the 8th week onward, may be regarded as composed of a large vein in the thoracolumbar line with the incorporated lower segment of the lumbar azygos vein. The nerves which pass forward from the sympathetic chain to the preaortic plexuses remain on the medial side of the inferior vena cava, and thus lie in the adult as in the embryo, between it and the aorta. If the lower segment of the lumbar azygos vein should persist in the adult, these nerves would be found between it and the inferior vena cava, and it would be continuous above with the communicating vein, which usually springs from the dorsal aspect of the inferior vena cava, and joins the thoracic azygos vein by traversing the aortic opening of the diaphragm.

It is evident that the normal position of the sympathetic nerves which in the human subject lie dorsomedial to the inferior vena cava precludes the possibility of the derivation of this part of the vena cava from an embryonic vein lying in the true azygos line. The lower, or caudal part of the “lumbar supracardinal” vein in the human subject, which gives rise to the first part of the inferior vena cava, thus according to the definition of these veins given by Reagan, lies in the thoracolumbar line, while the upper or cranial part of the “lumbar supracardinal”’ lies like the “thoracic supracardinal” vein in the true azygos line, since the greater and lesser splanchnic nerves lie ventrolateral to it. See text-fig. 1.

In the adult human subject a few sympathetic nerve fibres normally pass from the lower part of the lumbar sympathetic chain to the lateral part of the hypogastric plexus, in front of the common iliac vessels. This cireumstance, however, does not invalidate the general conclusion that that part of the inferior vena cava which extends from near its commencement to just below the termination in it of the renal veins does not occupy the true azygos line. In the embryo, as in the adult, the principal nerves from the sympathetic chain course forward to the preaortic, mesenteric and hypogastric plexuses, medial to the inferior vena cava, and between it and the abdominal aorta, Plate II, fig. 2, a few lie lateral to the pelvic part of the posterior cardinal vein and commencement of the umbilical artery. It is these nerves which in the adult pass in front of the common iliac vessels. If the inferior vena cava were developed in the true azygos line, it would lie dorsomedial to the principal sympathetic nerves or, in other words, these nerves, in order to reach the preaortic plexuses, would have to pass over instead of behind it.

The lower part of the left lumbar azygos vein, like that of the right side, is also incompletely developed in the human subject, and does not normally persist as a continuous longitudinal vessel. It probably takes part, however, in the transference of the left lumbar veins from their primary termination in the disappearing left inferior vena cava to the definitive right vein. The prevertebral or subcentral veins, according to Reagan and Strong, are also concerned in this temporary function.

The final course of the inferior vena cava in the human embryo appears to be determined about the 15 mm. stage, when the connection of the right supracardinal vein of Huntington with the right subcardinal vein is established. This important communicating vein is the supracardinal-subcardinal anastomosis of McClure and Butler. The general relations of the anastomosis will be realised by reference to Plate II, fig. 8, which represents a transverse section of a 22mm. human embryo. It will be noted that the right side has become enlarged so as to form the main venous channel, the “pars renalis”’ of the inferior vena cava, whereas the left side of the ‘“‘renal collar’ has already narrowed prior to its disappearance at a later stage.

The embryonic veins which take part in the formation of the inferior vena cava thus comprise:

(1) The right supracardinal (right paraureteric vein). This is a longitudinal axial vein in the thoracolumbar line, which is continuous caudally with the pelvic (somatic) part of the right posterior cardinal vein. It connects the lumbar intersegmental veins, and is situated between two series of sympathetic nerves: (a) nerves which lie lateral to the main venous channel (inferior vena cava) and pass in a dorsoventral direction from the sympathetic cord to the suprarenal and renal plexuses, and the lateral part of the hypogastric plexus; (b) nerves which are situated medial to the main vein (inferior vena cava) and pass in a dorsoventral direction from the sympathetic chain to the preaortic plexus and its derivatives, viz. the superior mesenteric, genital, and inferior mesenteric plexuses, and the central part of the hypogastric plexus (Plate II, figs. 8, 4). In the human subject the lower part of the right lumbar azygos vein appears to be incorporated into the main channel. This conception of the absorption of the lower part of the right lumbar azygos vein into the main venous channel is supported by the fact that the upper part of the right lumbar azygos vein in embryos above 20 mm. in length, and in the adult, springs from the dorsal aspect of the inferior vena cava.

(2) The supracardinal-subcardinal anastomosis.

(3) A part of the right subcardinal.

(4) The anastomosis of the right subcardinal vein with the common hepatic vein by means of the hepatic sinusoids. (5) The common hepatic vein.

Explanation of Anomalies

The explanation of the main features of the anomalous venae cavae described in this article are briefly as follows:

Specimens 1 and 2. Persistence on the left side of the corresponding embryonic veins, which normally give origin to the postrenal part of the right inferior vena cava, namely, the left supracardinal vein; the anastomosis of this with the left subcardinal vein; a part of the left subcardinal vein, and the intersubcardinal anastomosis, which joins the left with the right inferior vena cava.

Specimen 3. Persistence of the ventral limb of the circum-umbilical venous ring, and disappearance of its dorsal limb.

Specimen 4, Persistence of the whole of the postrenal segment of the left -subcardinal vein.

Specimen 5. Persistence and enlargement of postaortic anastomoses between the embryonic inferior venae cavae, and of one of the primary left renal veins.

The accessory renal artery and accessory renal veins in Specimen 4 are due to the persistence of primary embryonic renal vessels. These temporary or primary embryonic arteries and veins frequently penetrate or emerge from the medial aspect of the metanephros instead of traversing the hilum, which in the early stages of development is directed ventrally and thus does not afford a direct line of entrance_or exit for the vessels. The primary embryonic arteries supplying the right kidney usually pass ventral to the inferior vena cava, and between it and the subcardinal vein. One of these vessels has persisted in Specimen 4.

The tributary vein which joins the inferior polar vein of the right kidney in Specimen 4 is probably due to a persistence of one of the numerous veins which in the embryo drain the degenerating mesonephros. In early embryos when the kidney is low in position these vessels lie ventral to the metanephros; when the kidney has ascended into the lumbar position, the vessels are left in a subperitoneal position on the posterior abdominal wall below the level of the kidney.

A knowledge of the percentage frequency of a large vein situated on the left side of the abdominal aorta is of some surgical importance in connection with operations such as the Hunter-Royle method of treating spastic paralysis of the lower limbs by “lumbar sympathetic ramisection.”” The abnormal vein may be due either to double inferior vena cava, or a single left inferior vena cava. The latter may occur in transposition of the viscera, or may be due to persistence on the left side of the embryonic veins corresponding to those which normally give origin to the postrenal segment of the inferior vena cava on the right side.

The statistical material of which I have had personal knowledge is that which has come under my observation in the Anatomy Departments of the Middlesex Hospital Medical College and King’s College, London; and I am indebted to Prof. T. Yeates for the information with regard to the average number of subjects which have been used in the Anatomy Department of the Middlesex Hospital since his period of office in that Institution, during which no case of double or left inferior vena cava has occurred. I am thus enabled to add the number of subjects which have been dissected in the Department during this latter period to those which came under my observation in the same Institution beforehand. The total number of cases during the two periods is approximately 500, during which time one case of a large left inferior vena cava occurred, and no instance of a double inferior vena cava. During the period 1912 to 1928, in which I have been teaching in the Anatomy Department of King’s College, London, the number of subjects which have been dissected is 876, and two examples of bilateral postrenal vena cava have occurred.

The total number of cases examined and those in which a large vein is present on the left side of the abdominal aorta, including Specimen 4, is respectively:


Middlesex Hospital we wee 500 1

King’s College, London... wee 376 3. 876 4


These figures, which must be regarded as approximate only, give the percentage frequency of a large vein ascending on the left side of the abdominal aorta as 0-45. Double inferior vena cava appears to be about twice as frequent as single left inferior vena cava; a conclusion which is supported by a comparison of the figures given above with the proportional number of cases of each variety which have been published, and have been classified by Maxwell and Erwin (16) and by Wicke (25).

In conclusion I wish to express my high appreciation and indebtedness to the authors whose names I have included in the appended bibliography, and more especially to the works of Hochstetter, McClure and Butler. I wish to thank Prof. Blair, Dr Reagan and Miss Tribe for their valuable personal help.

I also wish to thank Mr Mitchell Smith, Mr Sourasky, Mr Glazebrook, Mr Hollenrake and Mr Kemp for help given in dissection and drawing of the specimens, and I further wish specially to acknowledge my indebtedness to the excellent work of Mr J. Weston, who has prepared most of my serial sections of human embryos.

Explanation of Plates I and II

Plate I

Fig. 1. Transverse section through an 11mm. human embryo, showing the positions of the posterior cardinal, thoracolumbar, and azygos lines of veins relative to the sympathetic cord and splanchnic nerves.

Ao. Aorta. 8. Sympathetic ganglion.

AzLV. Small veins situated in the SMA. Superior mesenteric artery. future azygos lines. SN. Sympathetic nerve.

MN. Mesonephros. SR. Suprarenal gland.

PCY. Posterior cardinal vein. ThLV. Thoracolumbar veins.

PrCV. Precostal vein. Fig. 2. Sagittal section of a 12 mm. human embryo to the right of the median plane, showing the junction of the temporary thoracolumbar vein with the. posterior cardinal vein at the level of the body of the 6th thoracic vertebra.

CHV. Common hepatic vein. ThLV. Thoracolumbar vein. This vein will be DL. Liver. replaced about the 15mm. stage by MN. Mesonephros. a vessel in the azygos line, viz. the PC. Posterior cardinal vein. thoracic azygos vein, or thoracic PPO. Pleuroperitoneal opening. supracardinal vein of Huntington and RL. Right lung. : McClure.

Fig. 3. Sagittal section of a 12mm. human embryo to the right of the median plane, showing an anastomotic vein joining the posterior cardinal vein with the thoracolumbar vein, at the level of the suprarenal body.

AnV. Anastomosing vein. MN. Mesonephros.

GG. Genital gland. PCV. Posterior cardinal vein. HS. Hepatic sinusoids. RL. Right lung.

ISV. Intersegmental veins. SR. Suprarenal gland. IVC. Inferior vena cava. ThLV. Thoracolumbar vein.

L Liver.

Fig. 4. Sagittal section of a 12mm. human embryo passing to the left of the median plane. It shows the termination in the left posterior cardinal vein of a tributary coming from the’ postrenal anastomosis, and coursing forward above the upper pole of the kidney. A similar but much larger vein is present on the right side. These vessels, and the longitudinal postrenal anastomosis, represent the posterior limb of the perinephric ring of Hochstetter. Note also the opening of the lumbar intersegmental veins into the postrenal anastomosis, and the relation of the latter and the kidney to the left common iliac artery.

AnV. Anastomotic vein, which pro- LCIIA. Commencement of umbilical artery. bably represents the primary P. __— Pancreas. termination of a lumbar inter- PCV. Posterior cardinal vein. segmental vein in the posterior St. Stomach. cardinal vein. WB. Mesonephros. ISV. Intersegmental veins. UA. Umbilical artery.

K. Metanephros.


Plate II

Fig. 1. Transverse section through a 19mm. human embryo, showing the relations of the thoracic azygos veins, and precostal veins to the sympathetic cord, greater and lesser splanchnic nerves and rami communicantes. The extent of the lateral displacement of the cranial end of the mesonephros at this stage is indicated by the position of the “coronary appendage” of the liver. The upper pole of the mesonephros lies just below this structure.

Ao. Thoracic aorta. NSp. Splanchnic nerves.

CAp. Coronary appendage of liver. NY. Right and left vagus nerves. C.X. Tenth rib. PrCV. Precostal vein.

DY. Ductus venosus. SR. Suprarenal gland.

IVC. Inferior vena cava (pars hepatica). St. Stomach.

GS. Ganglion of sympathetic chain. TAzV. Thoracic azygos veins.

L. Liver. VTh.X. Tenth thoracic vertebra. 92


Fig. 2. Transverse section through a 19mm. human embryo, passing through the abdominal aorta just above its bifurcation. The section shows a large vein entering the inferior vena cava on its ventral aspect. This vessel forms the ventral limb of the circum-umbilical ring round the origin of the right common iliac artery. Lumbar intersegmental veins pass forward to the inferior vena cava on each side of the sympathetic chain. The axial veins situated on the median side of the sympathetic chain and between the sympathetic nerves and lumbar arteries are the lumbar azygos veins. The inferior venae cavae lie lateral to the sympathetic nerves passing forward to the hypogastric plexus, and medial to the ureters.

ALV. Ascending lumbar vein. PGP. Preaortic plexus of veins terminating aa. Genital gland. above in the subcardinal veins. LA. Lumbar intersegmental arteries. RC. Ramus communicans. LIVC. Left inferior vena cava (pars RIVC. Right inferior vena cava (pars suprasupracardinalis). / cardinalis). LLAzV. Left lumbar azygos vein. RK. Right kidney. LY. Lumbar vein. SN. Sympathetic nerve. MN. Mesonephros. ST. Sympathetic trunk. U. Ureter.

Fig. 3. Transverse section through a 22 mm. human embryo at the level of the supracardinosubcardinal anastomosis. On the left side the anastomosing vessel has become constricted, prior to its disappearance at a later stage. The relation of the principal veins to the sympathetic chain and to the preaortic and renal ganglia is shown; and also the relation of the Jumbar intersegmental veins and subcentral vein to the lumbar arteries. The termination of the internal spermatic veins in the subcardinal veins is also indicated.

Ao. Abdominal aorta. LV. Lumbar intersegmental veins.

K. Kidney. PAoG. Preaortic ganglia.

LA. Lumbar intersegmental artery. RISpV. Right internal spermatic vein.

LISpV. Left internal spermatic vein. RSV. Right subcardinal vein.

LRG. Left renal ganglion. RSpV. Right supracardinal vein.

LSV. Left subcardinal vein. SG. Ganglion of sympathetic chain. . LSpV. Left supracardinal vein. - Sp-SCAn. Supra-subcardinal anastomosis.


Fig. 4.. Transverse section through a 22 mm. human embryo below the intersubcardinal anasto mosis, showing the relation of the lumbar azygos veins to the inferior venae cavae. On the right side the lumbar azygos vein is connected to the inferior vena cava by a communicating branch. It is probable that the lower parts of the lumbar azygos veins become incorporated in the inferior vena cava by the widening out of these communications. The azygos veins lie medial to the sympathetic chain, and ventrolateral to the lumbar arteries,

Ao. Abdominal aorta. ELV. Left lumbar intersegmental vein. cs@. Collateral sympathetic ganglia (renal). RISV. Right internal spermatic vein. Ga. Genital gland. : RIVC. Right supracardinal vein.

ISA. Internal spermatic artery. RK. Right kidney.

LA. Lumbar artery. RLV. Right lumbar vein.

LISV. Left internal spermatic vein. SCV. Right subcardinal vein.

LIVC. Left supracardinal vein. SG. Ganglion of sympathetic chain. DEK. Left kidney. Uz. Ureter.

LLAzV. . Left lumbar azygos vein.

References to Literature

(1) Burtuer, E. G., v. McCiurs, C. F. W. (1925).

{2} Burer, E. G. (1927). “The relative réle played by the embryonic veins in the development of the mammalian vena cava posterior.” Amer. Journ. Anat. vol. XXXIx, p. 267.

(3) Cameron, J. (1911). “Persistence of the left posterior cardinal vein.” Journ. Anat. Physiol. vol. XLV, p. 416. .

(4)(1915). “A specimen showing complete remains of the left superior vena cava, with the description of a venule, which represents the lost extrapericardiac portion of the left duct of Cuvier.” Journ. Anat. Physiol. vol. xL1x, p. 141.

(5) Frazer, J. E. S. (1924). “The development of the main veins of the trunk caudal to the duct of Cuvier.” Proc. Anat. Soc. of Great Britain and Ireland. Journ. Anat. vol. L1x, p. 99.

(6) (1925). “The formation of the left common iliac vein.” Proc. Anat. Soc. of Great Britain and Ireland. Journ. Anat. vol. ux, p. 485.

(7) Guapstone, R. J. (1906). “An acardiac foetus (Acephalus omphalositicus).” Journ. Anat. Physiol. vol. xu, p. 73.

(8) —— (1911). “A case in which the right ureter passed behind the inferior vena cava.” Journ. Anat. Physiol. vol. xiv, p. 225. (9) —— (1912). “A case of left inferiot vena cava.” ,Journ. Anat. Physiol. vol. xLvI, p. 220.

(10) Hocustetter, F. (1893). “Beitrige zur Entwickelung des Venensystems der Amnioten, (3) Séuger.” Morph. Jahrbuch. 20. Bd., 4. Heft, S. 543-648.

(11) Huwytineton, G. 8. and McCuurs, C. F. W. (1907). “Development of the postcava and tributaries in the domestic cat.” Proc. Ass. Amer. Anat. Anat. Rec. No. 3.

(12) Huntrveton, G. S. (1920). “The development of the veins in the domestic cat (Felis domestica) with especial reference (1) to the share taken by the supracardinal veins in the development of the postcava and azygos veins, and (2) to the interpretation of the variant conditions of the postcava and its tributaries as found in the adult.” Anat. Rec. vol. xx.

(13) Kerscuner, L. (1888). “Zur Morphologie der Vena cava inferior.” Anat. Anz. Bd. 3.

(14) Jounston, T. B. “Anomaly of the vena cava inferior; with a note on the relationships which help to determine the nature of anomalies of some of the abdominal systemic veins.” Journ. Anat. Physiol. vol. xLvu, p. 235.

(15) Lewis, F. T. (1902). “The development of the vena cava inferior.” Amer. Journ. Anat. vol. 1.

(16) Maxwe tt, E. V. and Erwin, G. S. (1928). “Four cases of anomalous inferior vena cava, with an explanation of their developmental origin.” Journ. Anat. vol. LxI, p. 84.

(17) McCionz, C. F. W. and Butter, E. G. (1925). “The development of the inferior vena cava in man.” Amer. Journ. Anat. vol. xxxv, p. 331.

(18) OxrRrEL, O. “Teilweiser Fortbestand der unteren Cardinalvenen bei einem Erwachsenen.” Anat. Anz. Bd. Lxv, 8. 312.

(19) Ratuxs, H. (1830). “Ueber die Bildung der Pfortader und der Lebervenen der Saugethiere.” Arch. f. Anat. u. Physiol. (Meckel’s).

(20) Rzaaan, F. P. and Rosrnson, A. (1926). “The later development of the inferior vena cava in man and in carnivora.” Proc. Anat. Soc. Great Britain and Ireland. Journ: Anat. vol. LXI, p. 482.

(21) Reagay, F. P. with Trisz, M. (1926). “The early development of the postrenal vena cava in the rabbit.” Proc. Anat. Soc. Great Britain and Ireland. Journ. Anat. vol. ux1, p. 480.

(22) Rosiyson, A. (1891). “Abnormalities of the venous system and their relation to the development of veins.” Studies in Anatomy, The Owens College, Manchester, vol. 1, p. 197.

(23) Sasin, F. L. (1915). “On the fate of the posterior cardinal veins, and their relation to the development of the vena cava and azygos in the embryo pig.” Carnegie Institute of Washington. Contributions to Embryology, vol. m1, No. 7.

(24) Srrona, M. T. (1925). “The derivatives of the posterior cardinal vein in the rat.” Anat. Record, vol. xxx1, p. 320.

(25) Wrox, A. (1927). ‘Ueber einen Fall von Inselbildung im Bereiche der hinteren Hohlvene (Vena cava posterior) und Durchtritt des rechten Harnleiters beim Erwachsenen.” Zeits. f. Anat. u. Entwicklungsgeschichte, Bd. txxxtv, S. 524.

(26) Zumsretm, J. (1896). “Zur Anatomie und Entwicklung des Venensystems des Menschen.” Anat. Hefte, Bd. vi.


For further references to literature on the development of the veins in animals, consult articles by McClure, Butler and Reagan; and for abnormalities of the inferior vena cava in man, see Maxwell and Erwin, and Wicke.




Cite this page: Hill, M.A. (2020, January 27) Embryology Paper - Development of the inferior vena cava (1929). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Development_of_the_inferior_vena_cava_(1929)

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