Paper - The development of the vena cava inferior in man (1925)

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McClure CFW. and Butler EG. The development of the vena cava inferior in man. (1925) Amer. J Anat. 35(3): 331-383.

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This 1925 paper describes human inferior vena cava development. This paper includes descriptions of the venous system of several Carnegie Collection human embryos as well as human embryos from the Harvard Collection and other collections.


Carnegie Collection: 588 (Carnegie stage 13) | 623 (Carnegie stage 17) | 841 (Carnegie stage 18)

See also earlier paper: Lewis FT. The development of the vena cava inferior. (1902) Amer. J Anat. 1(3): 229-244.

Heart - Historic References 
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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Tandler J. The Development of the Heart. (1912) Sect. II, chapt. 18, vol. 2, in Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia., pp. 534-570.

Mall FP. On the development of the human heart. (1912) Amer. J Anat. 13: 249-298.

Abbott ME. Congenital Cardiac Disease (1915) Osler & Mccrae's Modern Medicine 6, 2nd Edition.

Frazer JE. The formation of the pars membranacea septi. (1916) J Anat. 51(1): 19-29. PMID 17103800

Waterston D. The development of the heart in man. (1917) Trans. Roy. Soc. Edin., 7(2): 258-302.

McClure CFW. and Butler EG. The development of the vena cava inferior in man. (1925) Amer. J Anat. 35(3): 331-383.

Odgers PNB. The formation of the venous valves, the foramen secundum and the septum secundum in the human heart. (1935) J. Anat., 69: 412-422. PMID 17104548

Odgers PN. The development of the pars membranacea septi in the human heart. (1938) J Anat. 72(2): 247-59. https://www.ncbi.nlm.nih.gov/pubmed/17104688 PMID 17104688]

Patten BM. Developmental defects at the foramen ovale. (1938) Am J Pathol. 14(2):135-162. PMID 19970381

Odgers PNB. The development of the atrio-ventricular valves in man. (1939) J Anat. 73: 643-57. PMID 17104787

Kramer TC. The partitioning of the truncus and conus and the formation of the membranous portion of the interventricular septum in the human heart. (1942) Amer. J Anat. 71(3): 343-370.



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1902 Vena cava inferior | 1905 Brain Blood Vessels | 1909 Cervical Veins | 1909 Dorsal aorta and umbilical veins | 1912 Heart | 1912 Human Heart | 1914 Earliest Blood-Vessels | 1915 Congenital Cardiac Disease | 1915 Dura Venous Sinuses | 1916 Blood cell origin | 1916 Pars Membranacea Septi | 1919 Lower Limb Arteries | 1921 Human Brain Vascular | 1921 Spleen | 1922 Aortic-Arch System | 1922 Pig Forelimb Arteries | 1922 Chicken Pulmonary | 1923 Head Subcutaneous Plexus | 1923 Ductus Venosus | 1925 Venous Development | 1927 Stage 11 Heart | 1928 Heart Blood Flow | 1935 Aorta | 1935 Venous valves | 1938 Pars Membranacea Septi | 1938 Foramen Ovale | 1939 Atrio-Ventricular Valves | 1940 Vena cava inferior | 1940 Early Hematopoiesis | 1941 Blood Formation | 1942 Truncus and Conus Partitioning | Ziegler Heart Models | 1951 Heart Movie | 1954 Week 9 Heart | 1957 Cranial venous system | 1959 Brain Arterial Anastomoses | Historic Embryology Papers | 2012 ECHO Meeting | 2016 Cardiac Review | Historic Disclaimer
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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

The Development of the Vena Cava Inferior in Man

Charles F. W. Mcclure and Elmer G. Butler


Laboratory of Comparative Anatomy, Princeton University

Eighteen Figures (1925)

Introduction

A survey of the investigations dealing with the development of the inferior vena cava indicates that at the present time a detailed knowledge of the formation of this Vein in man is still lacking. N o definite published observations on human embryos appear to have been made since those of Hochstetter (’93) and Zumstein (’96). Inasmuch as the earlier observations on the development of the inferior Vena cava of mammals in general have been subjected to modifications as the result of the researches chiefly of F. T. Lewis (’02) and of Huntington and McClure (’07 and ’20), it has seemed desirable, in the light of the knowledge obtained by this more recent work, to make a more detailed study of a series of human embryos. The investigation made and set forth in the following pglgcs embodies a description of the plan of the venous system and its transformations, as observed in a carefully selected series of human embryos in which, we believe, are revealed all of the critical stages in the development of the inferior vena cava. A comparison and correlation of the arrangement of the Veins in each embryo with developmental stages in the cat already worked out in great detail by Huntington and McClure (’20) have made possible, we believe, a correct morphological interpretation of the conditions observed in man.


The absence of previous more detailed investigations on the development of the inferior vena cava in human embryos is somewhat surprising and has probably been due to the lack of a suflicient number of embryos of appropriate stages as well as to the comparative difliculty With which human material suitable for such a study is obtained. The present work has been carried out by the utilization of embryos Obtained from several collections, viz., the Carnegie Embryological Collection, the Embryological Collection of the College of Physicians and Surgeons (P and S) of Columbia University, the Embryological Collection of Cornell University Medical College, and the Harvard Embryological Collection. It is a. pleasure to acknowledge the kindness and courtesy of Prof. George L. Streeter, Prof. George S. Huntington, Prof. Charles R. Stockard, and Prof. Frederic T. Lewis for generously supplying us with excellent material for this work.


Numerous embryos have been examined, and those at important and critical stages were reconstructed in wax after the method of Born.


The following is the series of human embryos actually made use of in this investigation:

Carnegie Embryological Collection

Carnegie Embryological Collection (Baltimore)

  • No. 588, 4 mm embryo (reconstructed x 150)
  • No. 800, 6.5 mm embryo
  • No. 623, 10.1 mm embryo (reconstructed x 100)
  • No. 841, 15 mm embryo (reconstructed x 100)

Embryological Collection of the College of Physicians and Surgeons of Columbia University

(New York)

  • No. 1095, 11 mm embryo (reconstructed x 100)
  • No. 1024, 16 mm embryo (reconstructed x 100)
  • No. 1090, 22 mm embryo (reconstructed x 100)

Embryological Collection Of Cornell University Medical College

(New York)

  • 10.2 mm embryo
  • 14 mm embryo
  • 15 mm embryo
  • 19 mm embryo

Harvard Embryological Collection

Harvard Embryological Collection (Boston)

  • No. 2051, 15 mm embryo (reconstructed x 100)
  • No. 1913, 18 mm embryo (reconstructed by Huntington and McClure in 1915)
  • No. 2924, 25 mm embryo
  • No. 2128, 45 mm embryo (reconstructed x 50)


Owing largely to the circumstance of our obtaining material from these several collections, we found that the recorded length of the various embryos cannot always be taken as indicating exactly their relative ages. Our studies have shown that the embryos examined by us can be arranged, at least so far as the development of the venous system is concerned, in the following series according to age: 4 mm (Carnegie, no. 588); 6.5 mm (Carnegie, no. 800); 10.2 mm (Cornell); 11 mm (P and S, no. 1095); 10.1 mm (Carnegie, no. 623); 15 mm (Cornell); 15 mm (Carnegie, no. 841); 15 mm (Harvard, no. 2051); 14 mm (Cornell); 16 mm (P and S, no. 1024) ; 18 mm (Harvard, no. 1913) ; 19 mm (Cornell) ; 22 mm (P and S, no. 1090 ; 25 mm (Harvard, no. 2924) and 45 mm (Harvard, no. 2128). We have also observed that all of the really significant transformations of the embryonic veins, leading up to the establishment of the inferior vena cava, take place largely in embryos measuring approximately between 10 and 18 mm in length.


The figures of the actual reconstructions (figs. 2, 4, 6, 8, 10, 11, 13, 15, and 16) which accompany the following descriptions are fairly accurate representations of the reconstructed veins} In order to avoid confusion, however, and for the sake of exhibiting more clearly the more important veins, it has been deemed advisable to omit from the drawings a number of details actually present but not necessarily essential to explain the conditions at hand. Among the vessels omitted are, in figure 10, the lumbar cardinal collateral veins.


We wish to express our appreciation to Mr. M. Petersen, of the College of Physicians and Surgeons of Columbia University, for his accurate representations of our complicated reconstructions.


In addition, we submit a series of conventional diagrams (figs. 1, 3, 5, 7, 9, 12, 14, and 17) based on the series reconstructed, which show all the critical ontogenetic stages leading from the early Venous ground—plan, common to all mammals, to the conditions obtaining in the adult.

Although our studies have been confined chiefly to the development of the inferior vena cava and its more important tributaries, we have made observations also on the development of the azygos and hemiazygos veins, as the la.tter, together with the inferior vena cava, constitute in man, as in the cat, a morphologically inseparable system of veins. In constructing these diagrams we have included also the transformations of the ducts of Cuvier and of the anterior cardinal veins, as generally described in text-books of embryology. We fully appreciate, however, that the transformations we have associated with particular ages may not in all cases strictly apply to the embryo concerned.

4 mm Human Embryo

Carnegie Embryological Collection, no. 588. (figs. 1 And 2)

The venous system of this embryo has been previously reconstructed by Dr. George L. Streeter (publication 271 of the Carnegie Institution of Washington).

Streeter 1921  
Streeter GL. The developmental alterations in the vascular system of the brain of the human embryo. (1921) Contrib. Embryol., Carnegie Inst. Wash. 8:7-38.

This is the youngest embryo studied by us, and neither metanephroi nor sex glands, as such, are yet in evidence. Both omphalomesenteric veins (V.0m.) open into the sinus venosus (S.V.), While the ducts of Cuvier (D.C.) receive, respectively, the right and left umbilical veins ( V.Umb.). The posterior cardinal veins (Pc.) lie dorsal to the mesonephroi and are approximately bilaterally symmetrical, although the diameter of the left posterior cardinal is slightly greater than that of the vein on the right side. Both veins taper gradually toward the caudal end of the body. Each posterior cardinal vein (Pc.) joins cranially with the anterior cardinal (Prc.) to form the ducts of Cuvier D.C.) which open into the sinus venosus (S.V.). The subcardinal veins (Saba) lie medial to the mesonephroi and have not yet reached the height of their development. The right and left subcardinal veins join the posterior cardinals at the cranial ends of the mesonephroi and can be traced caudad along the cranial half of the latter. Anastomoses (Anast.Subc.Pc.) occur at intervals between the subcardinal and posterior cardinal veins, and both of these Veins also receive numerous small tributaries from the mesonephric tubules with which they lie in close contact. The posterior cardinal veins also receive the segmental veins from the body wall. These latter tributaries are not shown in the figures.


Such a venous plan as this embryo exhibits represents the basic embryonic arrangement common to all sauropsida and mammalia thus far investigated and has been termed by Huntington and McClure the cardino—subcardinal stage. Except for the presence of umbilical veins, this cardino-subcardinal stage also constitutes the basic ground~plan of the embryonic venous system in the lower vertebrates, where it similarly forms the starting—point of a series of modifications leading to the adult stage.


An examination of embryos between 4 mm (Carnegie Collection, no. 588) and 10.2 mm (Cornell Collection) in length shows that the arrangement of the posterior cardinal and subcardinal veins continues to be entirely symmetrical with little change, except in size. The subcardinal Veins, however, have extended farther caudad along the mesonephroi, and more prominent anastomoses have been established between the posterior cardinal and subcardinal veins. These changes are obviously necessitated by the increased volume of blood and are probably associated with the general increase in body size. It can therefore be stated that the general plan of the venous system in human embryos, up to approximately 10 mm in length, conforms to that of the cardino—subcardinal stage (figs. 1 and 2), in which all the blood from the mesonephroi and the region of the body caudal to the ducts of

Cuvier is returned to the heart by the posterior cardinal veins.

Explanation of Figures

The broken lines in figures 7, 9, 12, 14, and 17 indicate veins which have undergone complete degeneration.


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


Figures 1, 3, 5, 7, 9, 12, 14, and 17 are a series of diagrams, based on reconstructions made of the veins (figs. 2, 4, 6, 8, 10, 13, 15, and 16) illustrating the development in man of the inferior vena cava and its principal tributaries.

Abbreviations

Abbreviations  
McClure 1925 Paper Abbreviations

A., lumbar division of right posterior cardinal vein (V. cardinalis posterior dextra)

A.Coel., coeliac artery (A. coeliaca)

Adr., adrenal vein (V. adrenalis, suprarenalis)

A.Mes.Ant., anterior mesenteric artery (A. mesenterica anterior)

A.Mes.Inf., inferior mesenteric artery (A. mesenterica inferior)

A.Meson., branch of aorta to mesonephros (A. mesonephrica)

A.Om., omphalomesenteric (A . omphalomesenterica)

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

Anast.IL.Pc., anastomosis between posterior eardinal veins at level of iliac veins

Anast. Int. S prc., intersnpracardinal anastomosis. Anastomosis between supraeardinal veins

Anast. Pc.Sprc., posterior cardinalsupraeardinal anastomosis. Anastomosis between posterior cardinal and supracardinal veins

Anast. Subc.Pc., snbcardino-posterior cardinal anastomosis. Anastomosis between subeardinal and posterior cardinal veins

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

Anast. Subc.Sprc.D6;r.t. (R.Col. — .P.Ren.) , right subcardino-supraeardinal anastomosis (lateral portion, right side, of renal coll-ar—pars renalis of vena cava. inferior) artery

An.ast.Subc.Sprc.Si/n.., left subcardinosupracardinal anastomosis (lateral portion, left side, or renal collar)

Ao., aorta

Az., azygos vein (V. azygos)

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

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

0.0., ventral portion of circumumbilical venous ring (V. cardinalis collateralis)

O.S., coronary sinus (sinus coronarius)

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

D.C., duct of Cuvier

Dext., dextra

E.Ii. V., external iliac vein (V. iliaca externa)

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

Hep.Subc.J ct., hepato—subcardinal junction (junction made between hepatic sinusoids and right subeardinal vein)

I.ll.V., internal iliac vein (V. iliaca interna)

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

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

Jug.Int., internal jugular vein (V. jugnlaris interna)

K., permanent kidney (metanephros)

L.Imom.V., left innominate vein (V. anonyma sinistra)

Mes.Caud.Pc., a tributary of the posterior cardinal vein draining the caudal portion of the mesonephros (caudal mesonephric branch of posterior cardinal)

P.Hep., pars hepatica of vena cava inferior

P.Ren., pars renalis of vena. cam inferior

P.Sprc., pars supracardinalis of vena cava inferior

P.Subc., pars subcardinalis of vena cava inferior

P.Subc.(Subc.Dext.), pars subcardinalis of vena cava inferior (right subcardinal vein)

Po., posterior cardinal vein (V. cardinalis posterior)

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

P0.Me.s'., posterior cardinal vein draining cranial portion of mesonephros

Pc.I., thoracic division of posterior eardinal vein forming cranial end of azygos vein

Pc.2.Dext., the portion of right posterior cardinal vein entering into formation of right periureteric (perimetanephric) venous ring

Pc.2.Sin., the portion of left posterior cardinal vein entering into formation of left periureteric (perimetanephric) venous ring

Pro, anterior cardinal vein (V. cardinalis anterior)

Prev, anterior vena cava (V. cava anterior)

R.Col., lateral portion of renal collar (subcardino—supracardinal a.nastomosis)

Ren.I., embryonic renal vein which is attached to renal collar (V. renalis)

Ren.II., embryonic renal vein which is attached to supracardinal vein (V. renalis)

R.V., renal vein in figure 18 (V. renalis)

S'cl., subclavian vein (V. subclavia)

Sim, sinistra

Sprcn, supracardinal vein (V. supracardinalis)

Sprc.A2., thoracic or azygos division of supracardinal vein

Sprc.Dext.(P.Sprc.), right supracardinal vein (pars supracardinalis of vena cava inferior)

Sprc.Sin.(P.Sprc.) (fig. 17 only), left supracardinal vein (pars supraeardinalis of vena cava inferior sinistra)

Sprc. (X), median channel between right and left supracardinal veins in figure 16

Subc., subcardinal vein (V. subcardinalis)

Subc.Sin.(Adr.), left subcardinal vein (left adrenal or suprarenal vein). V. adrenalis or suprarenalis sinistra

Subc.Pc.Anast., subcardino-posterior cardinal anastomosis (anastomosis between subcardinal and posterior cardinal Veins, fig. 18)

Subc.Sp'ro.Anast., subcardino-supracav dinal anastomosis (anastomosis between subcardinal and supracardinal veins, fig. 18)

S.V., sinus venosus in figures 1 and 2; sex veins in figure 18

Urn, ureter

V.Lu-mb., lumbar vein (V. lumbalis)

V.om., omphalo-mesenteric vein (V. omphalomesenterica)

V.Umb., umbilical vein (V. urnbilica.)

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

A., lumbar division of right posterior cardinal vein (V. cardinalis posterior dextra)

A.Coel., coeliac artery (A. coeliaca)

Adr., adrenal vein (V. adrenalis, suprarenalis)

A.Mes.Ant., anterior mesenteric artery (A. mesenterica anterior)

A.Mes.Inf., inferior mesenteric artery (A. mesenterica inferior)

A.Meson., branch of aorta to mesonephros (A. mesonephrica)

A.Om., omphalomesenteric (A . omphalomesenterica)

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

Anast.IL.Pc., anastomosis between posterior cardinal veins at level of iliac veins

Anast. Int. S prc., intersnpracardinal anastomosis. Anastomosis between supracardinal veins

Anast. Pc.Sprc., posterior cardinalsupracardinal anastomosis. Anastomosis between posterior cardinal and supracardinal veins

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

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

Anast. Subc.Sprc.D6;r.t. (R.Col. — .P.Ren.) , right subcardino-supracardinal anastomosis (lateral portion, right side, of renal coll-ar—pars renalis of vena cava. inferior) artery

An.ast.Subc.Sprc.Si/n.., left subcardinosupracardinal anastomosis (lateral portion, left side, or renal collar)

Ao., aorta

Az., azygos vein (V. azygos)

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

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

0.0., ventral portion of circumumbilical venous ring (V. cardinalis collateralis)

O.S., coronary sinus (sinus coronarius)

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

D.C., duct of Cuvier

Dext., dextra

E.Ii. V., external iliac vein (V. iliaca externa)

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

Hep.Subc.J ct., hepato—subcardinal junction (junction made between hepatic sinusoids and right subcardinal vein)

I.ll.V., internal iliac vein (V. iliaca interna)

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

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

Jug.Int., internal jugular vein (V. jugnlaris interna)

K., permanent kidney (metanephros)

L.Imom.V., left innominate vein (V. anonyma sinistra)

Mes.Caud.Pc., a tributary of the posterior cardinal vein draining the caudal portion of the mesonephros (caudal mesonephric branch of posterior cardinal)

P.Hep., pars hepatica of vena cava inferior

P.Ren., pars renalis of vena. cam inferior

P.Sprc., pars supracardinalis of vena cava inferior

P.Subc., pars subcardinalis of vena cava inferior

P.Subc.(Subc.Dext.), pars subcardinalis of vena cava inferior (right subcardinal vein)

Po., posterior cardinal vein (V. cardinalis posterior)

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

P0.Me.s'., posterior cardinal vein draining cranial portion of mesonephros

Pc.I., thoracic division of posterior cardinal vein forming cranial end of azygos vein

Pc.2.Dext., the portion of right posterior cardinal vein entering into formation of right periureteric (perimetanephric) venous ring

Pc.2.Sin., the portion of left posterior cardinal vein entering into formation of left periureteric (perimetanephric) venous ring

Pro, anterior cardinal vein (V. cardinalis anterior)

Prev, anterior vena cava (V. cava anterior)

R.Col., lateral portion of renal collar (subcardino—supracardinal a.nastomosis)

Ren.I., embryonic renal vein which is attached to renal collar (V. renalis)

Ren.II., embryonic renal vein which is attached to supracardinal vein (V. renalis)

R.V., renal vein in figure 18 (V. renalis)

S'cl., subclavian vein (V. subclavia)

Sim, sinistra

Sprcn, supracardinal vein (V. supracardinalis)

Sprc.A2., thoracic or azygos division of supracardinal vein

Sprc.Dext.(P.Sprc.), right supracardinal vein (pars supracardinalis of vena cava inferior)

Sprc.Sin.(P.Sprc.) (fig. 17 only), left supracardinal vein (pars supracardinalis of vena cava inferior sinistra)

Sprc. (X), median channel between right and left supracardinal veins in figure 16

Subc., subcardinal vein (V. subcardinalis)

Subc.Sin.(Adr.), left subcardinal vein (left adrenal or suprarenal vein). V. adrenalis or suprarenalis sinistra

Subc.Pc.Anast., subcardino-posterior cardinal anastomosis (anastomosis between subcardinal and posterior cardinal Veins, fig. 18)

Subc.Sp'ro.Anast., subcardino-supracav dinal anastomosis (anastomosis between subcardinal and supracardinal veins, fig. 18)

S.V., sinus venosus in figures 1 and 2; sex veins in figure 18

Urn, ureter

V.Lu-mb., lumbar vein (V. lumbalis)

V.om., omphalo-mesenteric vein (V. omphalomesenterica)

V.Umb., umbilical vein (V. urnbilica.)

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

11 mm Human Embryo

Embryological Collection of the College of Physicians and Surgeons (P And S) of Columbia University, No. 1095. (figs. 3 and 4)


This 11-mm embryo is slightly older than the 10.2 mm embryo of the Cornell Collection, and in both of these embryos we meet, for the first time, with a critical modification of the basic embryonic Venous plan. This consists chiefly in a union, through the caval mesentery, between the hepatic sinusoids and the right subcardinal vein forming the hepato-subcardinal junction (Hep.Sub cf., figs. 3 and 4). The result is the establishment of the prerenal division of the inferior Vena cava which is formed from the vena hepatica communis of Hochstetter, the hepatic sinusoids, an independent Vein in the caval mesentery and a portion of the right subcardinal vein (F. T. Lewis). The prerenal portion of the inferior vena cava may therefore be conveniently described as consisting of two main embryonic subdivisions, the pars hepatica and pars subcardinalis (P.Hep. and P.Subc., in fig. 3).

McClure1925 fig01.jpg

Fig. 1 Diagram of the venous system of a 4 mm human embryo of the Carnegie Embryological Collection, no. 588.

McClure1925 fig02.jpg

Fig. 2 Reconstruction of the venous system of a 4 mm human embryo of the Carnegie Embryological Collection, no. 588.

McClure1925 fig03.jpg

Fig. 3 Diagram of the venous system of an 11-mm human embryo of the Embryological Collection of the College of Physicians and Surgeons (Columbia University), no. 1095.


In the 10.2 mm of the Cornell Collection no indication of an anastomosis between the two subcardinals, caudal to the level of the omphalo—mesenteric artery, could be determined.


In the 11 mm embryo of the P and S Collection, however, a vascular area is evident at this point (Anast.Int.Subc., figs. 3 and 4) and indicates a potential union between these two veins. This intersubcardinal anastomosis is met with at a relatively earlier stage of development in the cat than in man. It is of fundamental importance for the reason that it forms an essential pathway by which subsequently the blood becomes directed from the left side of the body to the prerenal division of the inferior vena cava. In any event, the establishment of the prerenal division of the inferior vena cava in these two embryos has caused the blood to be returned to the heart in part, at least, by a new pathway, other than the posterior cardinal veins.

McClure1925 fig04.jpg

Fig. 4 Reconstruction of the venous system of an 11-mm human embryo of the Embryological Collection of the College of Physicians and Surgeons (Columbia University), no. 1095.


In both of these embryos (10.2 and 11 mm) the posterior cardinal veins (Pu), lying dorsal to the mesonephroi, are still approximately bilaterally symmetrical. They extend as continuous vessels between the caudal end of the body and the point where, in common with the anterior cardinal veins (Pro), they open into the ducts of Cuvier. The caliber of each posterior cardinal differs along its course, being greater along the caudal two—thirds of the mesonephros than along the cranial third. In the embryo of the P and S Collection, an anastomosis, ventral to the caudal artery, has been formed between the right and the left posterior cardinal veins (Anast.Il.P(,-.). This anastomosis receives the right and the left caudal veins and has not yet been formed in the 10.2 mm embryo of the Cornell Collection.


The permanent kidneys (metanephroi, K in fig. 1) have made their appearance in both embryos. They lie ventral to the umbilical arteries with their caudal ends not far removed from the iliac anastomosis between the two posterior cardinals and with their cranial ends slightly caudal to the level of origin of the inferior mcsenteric artery from the aorta (A.Mc.9.Inf.). The presence of the permanent kidneys has brought about an important change in the character of the posterior cardinals, each of which now makes an abrupt. bend ventrad, forming an acute angle in the vein, at approximately the caudal end of each mesonephros. The cranial half of the metanephros lies closely pressed against the medial side of that portion of the posterior cardinal vein which extends dorsad and caudad of the acute angle above mentioned, and the vein at this point has become laterally compressed, due to the pressure exerted on it by the metanephros. This portion of the posterior cardinal vein, which lies lateral to the cranial half of the metanephros and labeled Pc.2 in all figures, in later stages undergoes profound changes in correlation with the formation of the supracardinal veins and the establishment of the postrenal division of the inferior vena cava.


The subcardinal veins in these two embryos are exceedingly difficult to follow in serial sections, even under high magnification. We found this to be true in the case of all human embryos of early stages. One reason for this difficulty is that such embryos are not ordinarily fixed While in a perfectlyfresh condition or in reagents by which the shrinkage of blood vessels is largely eliminated. The reconstruction of the subcardinal veins in the embryo of the P and S Collection which are really, for the most part, only capillaries, is quite accurately reproduced in figure 4, where the subcardinal veins appear to consist of a series of discontinuous vascular areas. Since we have been able to determine that in embryos younger than that of the P and S Collection the subcardinal veins are continuous and that in later stages they are invariably so, We may assume that in the embryo in question we are dealing at this stage with a continuous system of vessels.


In addition to the vascular area present between the subcardinals, caudal to the origin of the omphalo-mesenteric-artery (Anast.Int.Subc., figs. 3 and 4), between the posterior cardinal and subcardinal veins are found a number of connections (Auast.Subc..Pc.) which lie dorsal to the mesonephroi, and on each side of the body is found an especially prominent one which arches round the caudal end of the mesonephros. We have mentioned above the presence in each posterior cardinal vein of an acute bend at about the level of the caudal end of each mesonephros. Extending caudad from this bend, and located ventral to the main posterior cardinal channel, we have observed for the first time a small vein which has been termed by us the caudal mesonephric branch of the posterior cardinal (Mes.C-'aud.Pc., figs. 3 and 4) for the reason that in later stages it serves to convey blood from the caudal end of the mesonephros to the posterior cardinal vein.

10.1 mm Human Embryo

Carnegie Embryological Collection, No. 623. (figs. 5 And 6)

This embryo is slightly older than either of the two preceding embryos mentioned, belonging, respectively, to the Cornell and P and S Collections. This can be determined by the presence of a more extensive anastomosis between the posterior cardinals at their iliac junction (Anast.Il.Pc.); by the presence of a more definite anastomosis between the subcardinals, caudal to the level of origin of the omphalo—meseteric artery from the aorta (A-nu-st.I'nt.Subc.); by the slight cranial extension of the metanephroi, the caudal ends of which now lie opposite to and not caudal to the level of origin of the umbilical arteries, and by the beginning atrophy of the left posterior cardinal vein. In all other respects the general plan of the vinous system in this 10.1 mm embryo conforms to that observed in the 11 mm embryo of the P and S Collection (no. 1095).


As a result of the changes above noted, however, profound differences are observed in the relative value of certain vessels as pathways by which blood can now be returned to the heart from the caudal portion of the body. The atrophied condition of the left posterior cardinal vein and the establishment of a more definite intersubcardinal anastomosis have caused the blood, to a large extent, to be directed toward the prerenal division of the inferior vena cava (pars subcardinalis and pars hepatica) from the left side of the body, while the increased size of the anastomosis between the posterior cardinals at their iliac junction (Anast.Il.Pc.) has similarly caused the blood from the left lower limb bud to be directed into the right posterior cardinal vein (Pc.Dewt.), which now constitutes the principal pathway of the body. While blood may still be returned to the heart from the caudal portion of the body by three main pathways (right and left posterior cardinal Veins and prerenal divisions of the inferior cava), it is evident that the plan of the Venous system exhibited by this particular embryo foreshadows the asymmetrical plan characteristic of the adult.

McClure1925 fig05.jpg

Fig. 5 Diagram of the venous system of a 10.1 mm human embryo of the Carnegie Embryological Collection, no. 588. (Carnegie stage 17)


In View of their bearing on future transformations, other details of the venous plan of this embryo should be noted.

McClure1925 fig06.jpg

Fig. 6 Reconstruction of the venous system of a 10.1 mm human embryo of the Carnegie Embryological Collection, no. 588. (Carnegie stage 17)


The bend in the posterior cardinal Veins at the cranial end of the metanephroi (fig. 6) is still a marked feature and the same close relations still exist at this point, as in the 11 mm embryo of the P and S Collection, between the cranial end of the metanephros and the posterior cardinal, except that, on the left side of the body, the vein (Pc.2,Sm.) is much atrophied and is of relatively small size.


On the left side of the body the umbilical artery is encircled by a venous ring formed dorsally by the caudal end of the posterior cardinal and ventrally by a channel (C.C.) which extends between the latter and the iliac anastomosis formed between the posterior cardinal veins (Ana,st.Il.Pc.). Traces of a similar ventral channel are evident on the right side, but the shrunken condition of the vessels in this region has made it impossible to determine its presence with certainty. The presence of similar circumumbilical venous rings has been observed in a number of other cases as follows: In reptiles, by Hochstetter (’92); in birds, by Miller (’03); in marsupials, by McClure (’06) ; in the rabbit, by F. T. Lewis (’O2), and in the cat, by Huntington and McC-lure (’20). The presence of the ventral element of circumumbilical venous rings (C.C.) in the embryos of placental mammals therefore represents a condition of considerable morphological interest, since it forms the caudal continuation of a system of veins (cardinal collateral) which, though evanescent in character in placentals, is highly developed in marsupials where the cardinal collateral Veins enter into the formation of the posterior vena cava. As in marsupials, the cardinal collateral veins have been observed by Huntington and McClure in cat embryos where, in the lumbar region, they form an essentially continuous system of vessels ventrolateral to the aorta and extending between the intersubcardinal anastomosis and the iliac junction formed between the posterior cardinal veins.

15 mm Human Embryo

Carnegie Embryological Collection, No. 841. (figs. 7 And 8)


The stage of development represented by this embryo is possibly slightly more advanced than that of the 15 mm embryo of the Cornell Collection and marks the beginning of a series of transformations which lead directly to the establishment of the postrenal division of the inferior vena cava (pars renalis and pars supracardinalis) as met with in the adult. These transformations are chiefly associated with a gradual shifting of the blood current from the posterior cardinal Veins to the prerenal division of the inferior vena cava, in correlation with the appearance of a new set of Vessels known as the supracardinal system of veins.


The pars subcardinalis of the inferior Vena cava (P.Subc.) has increased in size and the posterior cardinal Veins (Pc.) have decreased accordingly, so that at the point Where the former enters the liver the caliber of the right subcardinal (P.Subc.) is now almost as great as that of the right posterior cardinal at the same level.

McClure1925 fig07.jpg

Fig. 7 Diagram of the venous system of a 15 mm human embryo of the Carnegie Embryological Collection, no. 841. (Carnegie stage 18)


The anastomosis between the subcardinals (An/ast.Imf.Subc.), caudal to the origin of the omphalo—mesenteric artery from the aorta (A.0m.), has also enlarged so that blood may now pass more freely from the left posterior cardinal to the prerenal division of the inferior Vena cava, by way of the subcardino—posterior cardinal anas— tomoses (Amtst.Subc.Pc.) and the intersubcardinal anastomosis (Auast.I1zt.Subc.).

McClure1925 fig08.jpg

Fig. 8 Reconstruction of the venous system of a 15 mm human embryo of the Carnegie Embryological Collection, no. 841. (Carnegie stage 18)


All conditions, therefore, point toward a progressive importance of the prerenal division of the inferior vena cava and a gradual loss in the role played by the posterior cardinal veins.


Especially important in our study of this embryo is the introduction of the supracardinal system of veins which in the cat has been shown by Huntington and McClure (’07~’20) to play an important role in the development of the postrenal division of the inferior vena cava and azygos veins. On each side of the body, in both the thoracic and lumbar regions, the supracardinal veins lie dorsolateral to the aorta and do not at this, as at a later stage, form a continuous system connecting these two regions. Appearing in man, as they do in the cat, in these two separate regions of the body, the supracardinal veins in the lumbar region cannot be regarded as merely a synonym for the dorsal limb of the periureteric venous rings first described by Hochstetter, but rather they comprise a morphologically uniform system of longitudinal channels which develop parallel to the posterior cardinal veins and ultimately contribute to the establishment of the azygos veins and a portion of the postrenal division of the inferior vena cava (pars supracardinalis).


In this 15-mm embryo of the Carnegie Collection the supracardinal veins in the thoracic region are bilaterally symmetrical and are essentially of the same caliber (8'prc.Az., fig. 7). Each vein joins the posterior cardinal at a point slightly craniad of the cranial end of the mesonephros and can be traced caudad to about the level of the hepato—sub— cardinal junction (Hep.S'ubc.Jct., fig. 7). The portion of the right posterior cardinal vein near the duct of Cuvier (D.C.) and cranial to its union with the right supracardinal (S'prc.Az.Dea;t.) constitutes in man, as in the cat, the only portion of the posterior cardinal vein which ordinarily enters into the formation of the adult azygos.


In the thoracic region the body wall is drained by a series of segmentally arranged vessels which at first are connected with the posterior cardinal veins. With the gradual atrophy of the latter, this segmental drainage becomes transferred to the supracardinal Veins, and this transfer has been largely accomplished in this embryo. The thoracic supracardinal veins lie relatively close to each other and intersupracardinal anastomoses which arise between them have not yet made their appearance in this 15 mm embryo.


In the lumbar region the supracardinal Veins (Sprc.Dcwt. and Sin.) are also bilaterally symmetrical and essentially of the same caliber. Each vein may be traced craniad to a point about opposite the cranial border of the intersubcardinal anastomosis (Anast.Int.Subc.), at which level prominent anastomoses are still in evidence between the posterior cardinal and supracardinal Veins (A'nast.Pc.Sprc.). The presence of these anastomoses indicates the manner of origin of the supracardinals in this region through a. longitudinal anastomosis between the dorsal tributaries of the posterior cardinals, as well as the manner in which these tributaries become transferred to the supracardinal veins.


Associated with the formation of the supracardinal veins in the lumbar region is the institution of an important channel on each side of the body,. by means of which the supra— cardinal vein establishes a connection with the prerenal division of the inferior vena cava. This vessel, the subcardinosupracardinal anastomosis (Anast.Subc.Sprc.Demt. and Sin.) extends ventrad, in a craniocaudal direction, along the medial surface of the cranial half of each metanephros, between the supracardinal vein and a subcardino—posterior cardinal anastomosis (Amzst.Subc.Pc.), with which, in common, it joins the intersubcardinal anastomosis (A%ast.Int.Subc.). As in the eat, this subcardino—supracardinal anastomosis, on each side of the body, enters into the composition of the lateral portion of the embryonic renal collar, a circumaortic venous ring formed at a later stage at about the level of the intersubcardinal anastomosis, and, on the right side, it finally enters into the formationof the pars renalis (P.Ren.) of the inferior vena cava. The reader should consult the composite diagram of the embryonic veins in the cat (fig. 18), which shows that the same morphological plan exists in man, as in the cat, as regards the formation of the embryonic renal collar.


As shown in figure 7, the right supracardinal vein in the lumbar region unites caudally with the posterior cardinal at a point slightly cranial to the origin of the umbilical arteries from the aorta. Blood may now be returned through channels on the right side of the body, directly to the heart from the iliac anastomosis between the posterior cardinals (Anast.ll.Pc.), either by the right posterior cardinal (Pc.2,De.rt.), or, to the prerenal division of the inferior vena cava, by way of the right supracardinal Vein (Sprc..De;vt.) and right subcardino-supracardinal anastomosis (f1‘WraSt.AS'Ub(:7. Spr(7.Dea;t.). On the right side, therefore, all of the embryonic subdivisions which enter into the formation of the adult inferior yena cava have been laid down and are as follows: Pars supracardinalis (Sprc.I)ecct.,P.Sprc.); pars renalis (Anast.Subc.Sprc.I)e.rt.,P.Ren., right side of renal collar); pars subcardinalis (Anast.I*nt.Subc. and I’.S'ubc.Dcac2f.) and pars hepatica (P.Hep.).


Associated with the appearance of the supracardinal Veins, a complete and typical venous ring has been formed about the metanephros on the right side of the body. 011 the medial side of the metanephros, as in the eat, this Venous ring is composed of a portion of the supracardinal Vein (Sprc.Dext.) and of the subcardi11o—supracardinal anastomosis (Anast. Sub('.Sprc.De9ct.) and, on the lateral side, of the posterior cardinal Vein (Pc.2, Deact.) and a portion of the subcardino—posterior cardinal anastomosis (Anast.Subc.Pc.Dcxt.). The long arrow X in figure 7 indicates the relations which the right metanephros and its ureter hold with respect to the component parts of the periureteric or, more strictly speaking, perimetanephric Venous ring, as observed in the 15-mm embryo of the Carnegie Collection. The reader is referred to figure 18, in which a periureteric Venous ring of exactly the same character is found in the cat.


The mesonephroi extend farther caudad in the 15 mm than in the 10.1-mm embryo of the (Jarncgie Collection. The result is that the caudal portion of tlie right mesonephros is now drained by the caudal mesonephric branch of the posterior cardinal (Mes.Caud.Pc.I)eact.), which has become a prominent branch of the posterior cardinal vein. This tributary joins the posterior cardinal where the latter bends ventrad (fig. 8) to form an acute angle, at a point somewhat cranial to the point of union between the right posterior cardinal and the right supracardinal veins. The portion of the right posterior cardinal between these two points, in all figures labeled Pc.2, lies closely pressed against the lateral surface of the right metanephros. The complete atrophy of this portion of the posterior cardinal on the left side of the body of this embryo (Pc.2,Sin., fig. 7), now clearly explains how the left caudal mesonephric branch of the posterior cardinal (Mes. C'aud.Pc.Sm.) has here become the direct caudal continuation of the left posterior cardinal vein and why the left supracardinal (Spr0.Sm.) connects directly with the iliac anastomosis between posterior cardinal veins (Anast.Il.Pc.). As the result of the complete atrophy of this portion of the left posterior cardinal (Pc.2,Sin.), a perimetanephric venous ring is not found on the left side of this embryo, although one might reasonably infer that a ring is present at a slightly earlier stage of development. The loI1g arrow Y i11 figure 7 indicates the relations which in this embryo the left metanephros and its ureter hold to the veins on the left side.


Cranial to the intersubcardinal anastomosis (Anastlnt. Subs.) a portion of the right subcardinal (Subc.Dea3t.), not concerned in the formation of the prerenal division of the inferior vena eava, joins the latter at the hepato-subcardinal junction (Hep.Subc.Jct.), while the left subcardinal in this region (Subc.Sm.) joins caudally with the intersubcardinal anastomosis. Both of these veins in succeeding stages of development become more closely associated with the adrenal bodies and, on the left side, the original embryonic subcardinal is retained in the adult as the adrenal (suprarenal)


Caudal to the intersubcardinal anastomosis, both subcardinal veins have retained their individuality and continuity as observed in earlier stages. In this respect they differ widely from the conditions found in the embryo of the cat, in which, through fusions with the posterior cardinal veins at frequent intervals, their individuality is soon completely lost.

15 mm Human Embryo

Harvard Embryological Collection, No. 2051. (figs. 9, 10, And 11)


On account of its excellent preservation, this embryo is perhaps the most perfect one studied by us and almost all of the blood vessels could be followed in great detail and without difficulty in every_region of the body. Certain de~ tails which in some of the other embryos could not be fully determined are here clearly displayed, such as the circumumbilical venous rings and the lumbar division of the cardinal collateral veins. While this embryo measures the same in length as embryo no. 841 of the Carnegie Collection, the stage of development represented by it is slightly more advanced. In general, the principal advance in development emphasized by it is the attainment of the typical asymmetrical plan of the adult, wherein, on the right side of the body, the inferior vena cava, along its entire extent, has now become the principal venous pathway of the body. As we shall see, this condition has been brought about by a still further atrophy of the posterior cardinal veins.


The caliber of the prerenal division of the inferior vena cava (P.Hep. and P.Subc., figs. 9 and 10) has greatly increased in size and is now much greater than that of either of the two posterior cardinal veins (Pc.D€.90t. and Sin.) which still unite with the ducts of Cuvier (D.C.), at the cardino— Cuvierian junction, in common with the anterior cardinal veins (Pro). The intersubcardinal anastomosis (A4/1.ast.Im‘.. Subc.) has also, for the most part, lost its original plexiform character and now appears to form a more definite portion of the main caval channel than was observed in the 15 mm embryo of the Carnegie Collection.


In the thoracic region the general plan of the supracardinal veins remains the same as in the Carnegie embryo, no. 841, except that these veins (Sprc.Az., fig. 9) can now be traced as far caudad as the level of the intersubcardinal anastomosis, where they appear to be directly continuous with the cranial extension of the lumbar supracardinal veins, at least on the right side.

McClure1925 fig09.jpg

Fig. 9 Diagram of the venous system of a 15-mm human embryo of the Harvard Embryological Collection, no. 2051.


In the lumbar region the general plan of the supracardinal Veins (Spraflext. and Sm, figs. 9 and 10) and of the union made by them, through the subcardino—supracardina1 anastomoses (A4zast.Subc.Sprc.Dext. and Sm.) with the prerenal division of the inferior Vena cava, remains also unchanged. A great difference now exists, however, in the relative value of these two pathways on opposite sides as a means of conveying blood from the iliac anastomosis between the posterior cardinals (Anast.Il.Pc.) to the prerenal division of the inferior vena cava. In the Harvard embryo the vessel on the right side has greatly increased in size and now possesses a caliber several times as great as that of the corresponding vessel of the opposite side. As clearly shown in figure 9, practically all the blood from the iliac anastomosis (Anast. Il.Pc.) is now returned to the prerenal division of the inferior vena cava by the vessel of the right side, a vessel which constitutes the definite postrenal division of the inferior vena cava and which is composed of the right supracardinal (Sp-rc. Dexf.,P..Sp-rc.) and right subcardino—supracardinal anastomosis (Anast.Subc.Sprc.,R.C0l.,P.Ren.). The increased size of this channel on the right side now definitely establishes the typical asymmetrical ven0u.s plan and, as we shall find in succeeding stages, this asymmetry becomes still further emphasized, in relation toga progressive atrophy of the posterior cardinal veins.

McClure1925 fig10.jpg

Fig. 10 Reconstruction of the venous system of a 15 mm human embryo of the Harvard Embryological Collection, No. 2051. Ventrolateral aspect.


McClure1925 fig11.jpg

Fig. 11 Reconstruction of the venous system of a 15 mm human embryo of the Harvard Embryological Collection no. 2051. Dorsolateral aspect showing periureteric (perimetanephric) venous ring of right side.


A longitudinal plexus has been established in the lumbar region of this embryo, on each side of the aorta, in connection with the supracardinal veins (fig. 11), and, as yet, no anastomosis has occurred, dorsal to the aorta, between the Vessels of opposite sides. This venous plexus forms the caudal continuation in the lumbar region of the cranial extension of the lumbar supracardinal and hence of the azygos veins (Sprc. Deaot, fig. 11). By a ventral extension of this plexus in the lumbar region a right and a left longitudinal channel, lying ventrolateral to the aorta, has also been formed. These two channels occupy a position identical with that of the marsupial embryonic cardinal collateral veins which, by their fusion ventral to the aorta, contribute in these animals to the formation in the adult of the posterior caval vein (McClure, ’06). W-‘Vliile these cardinal collateral veins are evanescent in character both in the cat and in man, they nevertheless possess a definite morphological significance and have an important potential value in explaining certain recognized variant conditions of the adult venous system already observed in the cat and in man. As previously described in connection with the 10.1-mm embryo of the Carnegie Collection (no. 623), circumumbilical venous rings (C.C., figs. 9 and 10) are in this embryo present on both sides of the body. While a direct continuity could not definitely be determined between the ventral circumference of the venous ring (C'.C'.) and the cardinal collateral channels in the lumbar region, the relations are such that a connection between the two could easily be established so that under certain conditions this entire system of vessels might continue to function at a still later stage. For reasons already mentioned in the first part of this paper, the cardinal collateral veins of the lumbar region are not shown in the diagrams or in the figures of the reconstructions.


A perimetanephric venous ring (figs. 9, 10, and 11), of exactly the same composition and holding the same relations to the metanephros as in the 15-mm Carnegie embryo, is still present in this embryo on the right side. The long arrow X in figures 7 and 9 indicates clearly the position occupied in these two embryos by the right metanephros and its ureter with respect to the veins. While the morphological plan of the metanephric venous ring is exactly the same in both embryos, a marked difference exists in the relative size and consequent functional value of that portion of the ring, formed by the right posterior cardinal vein (Pc.2,Deaot., fig. 11), which lies across the lateral surface of the metanephros. In the embryo of the Carnegie Collection (figs. 7 and 8) this portion of the posterior cardinal (Pc.2,Deact.) is of relatively large size, whereby a large volume of blood is permitted to pass from the iliac anastomosis (An/ast.Il.Pc.) direct to the heart, by way of the right posterior cardinal vein. In the Harvard embryo (figs. 9, 10, and 11), on the other hand, this portion of the right posterior cardinal (Pc.2,Dewt.) has undergone an extensive atrophy, so that the main volume of blood from the iliac anastomosis (Anrast.Il.Pc.) is directed no longer into the right posterior cardinal, but rather into the postrenal divisioniof the inferior vena cava, which has greatly increased in size.


In the 15-mm Harvard embryo an interesting condition is in process of being established whereby the Venous drainage of the caudal portion of the mesonephros is transferred from the posterior cardinal to the subcardinal veins. On the right side of the body the caudal mesonephric branch of the posterior cardinal vein (Caud.Mes.Pc.Dext.) has become greatly atrophied, so that blood from the caudal portion of the mesonephros is now, for the most part, directed to the heart through the right lumbar subcardinal (Subc.De9ct.) and prerenal division of the inferior vena cava, instead of, as in the 15 mm embryo of the Carnegie Collection, through the right posterior cardinal vein. That portion of the right posterior cardinal which extends craniad of its union with the caudal mesonephric branch of the posterior cardinal ( M es.Caud.Pc.) still remains, however, a vessel of considerable size and, as stated above, can be traced craniad where it joins the duct of C-uvier, It receives blood from the cranial portion of the mesonephros and still retains a connection with the intersnbcardinal anastomosis (Anast.Im‘.S'ubc.) by means of a muchatrophied subcardino—posterior cardinal anastomosis (Anasf. Subc.Pc.Dca3t.) which enters into the composition of the lateral circumference of the perimetanephric venous ring.


0n the left side of the body the cranial division of the posterior cardinal can still be followed to the duct of Cuvier, but has become atrophied to such an extent that the main volume of blood from the caudal portion of the mesonephros is no longer directed to the heart, as in the 15-mm embryo of the Carnegie Collection, through the left posterior cardinal, but rather into the prerenal division of the inferior vena cava by way of the left subcardinal vein (Subc.Sin.), through the greatly enlarged anastomoses present between the latter a11d the caudal mesonephric branch of the left posterior cardinal vein (M es.Caud. Pc.S-i.n.).


As compared with that of the cat, a striking feature of man’s development is the progressive importance of the lumbar division of the embryonic subcardinal veins which retain their primary individuality throughout all stages of development and, as we shall see, in the adult enter directly into the composition of the sex veins (Vv. spermaticae internae).


The adrenal organs are still drained by the subcardinal veins. On the left side the subcardinal vein (Sub‘c.A(Zr.S'm.) is relatively large and opens into the median anastomosis between subcardinal veins (A11-ast.ln—t.Subc.). On the right side several small veins from the adrenal organ (Adr.I)ea5t.) now open into the pars subcardinalis of the inferior vena cava (P. S~u-be-.), a11d in all probability one of these veins, or a. vein of this cl1a.racter, is retained in the adult as the right adrenal (suprarenal) vein.

16 mm Human Embryo

Embryological Collection Of The College Of Physicians And Surgeons (P And 8) Of Columbia University, No. 1024. (figs. 12 And 13)


A study of this embryo shows that between this and the 15-mm embryo of the Harvard Collection the difference in age is greater than the difference in measurement would indicate. While the 14-mm embryo of the Cornell Collection appears to represent a transition stage between the 15-mm Harvard embryo (no. 2051) and that of the P and S Collection (no. 1024), only the latter was reconstructed in wax, as it obviously illustrates the manner in which certain fundamental transformations have been accomplished in relation to a" still further atrophy of the posterior ca.rdinal veins.


The principal features illustrated by this 16-mm embryo are the increased size of the inferior vena cava, along its entire extent, and the almost complete atrophy of the right and the left posterior cardinal veins. As the transformations observed are largely related to a further modification of the early drainage plan of the posterior cardinal veins, we may first. consider the changes which these veins have undergone. By comparing figure 12 with figure 9, it will be observed in the 16-mm embryo that the posterior cardinal veins (Pc.) no longer form continuous vessels which convey blood from the caudal portion of the body to the ducts of Cuvier (D.C~'.). In the thoracic region only the proximal portion of the posterior cardinal veins, near the ducts of Cuvier, has been retained (P('.Az.) as the cranial extension of the supracardinals, now paired azygos veins (Spr¢:'.Az.), in addition to a more caudally situated portion (P«.:.Mes.), by which blood from the cranial end of the mesonephroi still drains into the ducts of Cuvier by way of the posterior cardinal veins.


In the lumbar region ‘that portion of the right. posterior cardinal (Pc.2,I)e;z:t.'),' present in the 15-mm Harvard embryo, which enters into the composition of the lateral circurnferenee of the perimetanephric venous ring, has completely disappeared. The only portion of the right posterior cardinal now metwith inthe lumbar region of this 16-mm 'embryo,is a much atrophied vessel (Pc.Dext.) directly continuous caudad, as iii the 15-mm Harvard embryo, with the caudal mesonephric branch of the posterior cardinal (M es.C'aud.Pc.Dea;t.) which drains into the right subcardinal Vein (S’ubc.Dext.). Except for a small amount of blood that passes through two primary connections (Anast.Subc.Pc.) still retained between this remnant of the right posterior cardinal and the inferior Vena cava, the blood from the caudal portion of the right mesonephros is now returned to the prerenal division of the inferior vena cava by the right subcardinal vein (Subc.Deaot.).


McClure1925 fig12.jpg

Fig. 12 Diagram of the venous system of a 16 mm human embryo of the Embryological Collection of the College of Physicians and Surgeons (Columbia University), no. 1024.


McClure1925 fig13.jpg

Fig. 13 Reconstruction of the venous system of a 16 mm human embryo of the Embryological Collection of the College of Physicians and Surgeons (Columbia University), no. 1024.


On the left side of the embryo the Venous drainage plan of the mesonephros in the lumbar region is essentially the same as on the right side. As blood can no longer reach the heart by way of the posterior cardinal, it is now directed from the left mesonephros to the prerenal division of the inferior vena cava by way of the left subcardinal vein (Siub(j-.iS'i21,.).


As a result of these modifications in the primary embryonic venous plan, it is evident that all the blood from the region of the iliac anastomosis between the posterior cardinals (A7zast.II.P('.) must now necessarily reach the prerenal division of the inferior vena cava by way of two veins. These are the postrenal division of the inferior vena cava (I’.Spirc. and P.Ren.), the larger of the two, and its l1omo— logue on the left side (Sprc.Sin. and Awast.S14I)('.Spr(?.Sin.). As in the 15 mm Harvard embryo, each of these veins makes an abrupt bend, in a cranioventral direction, in the region of the renal collar (A«nasf.Subc.Spr('.), before joining the prerenal division of the inferior vena cava at the intersubcardi— nal anastomosis (A4'l(lSf.I‘IZf.S’ubC.). Except that these two bilaterally situated channels are still present, the typical asymmetrical plan of the adult venous system in the lumbar region has now been attained.


If we attempt more closely to analyze the functional role played by the embryonic veins in bringing about this asymmetrical plan, we find that the presence of the impaired prerenal division of the inferior vena cava on the right side of the body is now associated witha general tendenc_v for the blood flow to be directed toward the right side, where finally it is collected by this increasingly important unpaired vein and is so conveyed to the heart. All of the transformations of the veins thus far described would therefore seem to represent a progressive series of stages in which the blood flow is gradually being directed from an originally bilateral system of vessels to this newly formed unilateral vessel on the right side, designated as the prerenal division of the inferior Vena cava.


As compared with the conditions observed iii the cat, in which the right and the left posterior cardinal veins in the lumbar region are retained as functional vessels until a relatively late stage, a striking feature of man’s development is the relatively early disappearance of both of these veins. Compare figure 5 of a 16-mm cat embryo in Huntington and McC-lnre’s publication with figure 12 of a 16 mm embryo of man.


In connection with this 16 mm embryo there remain to be mentioned the relations of the supracardinal veins in the thoracic region, and the position which the metanephroi now occupy with respect to the veins.

Both supracardinals (Spr(.r.Az.) are still present in the thoracic region and are directly cont.inuous candad with the cranial extension of the lumbar supracardinal Veins, so that, independently of the main caval line, blood can reach the heart from the caudal portion of the body through the supracardinal (azygos) veins. In both the thoracic and the lumbar regions, intersupracardinal anastomoses (A/nast.lm‘/.Spr(’., fig. 13), lying dorsal to the aorta, have been formed. These anastomoses are by no means so prominent, however, as those observed in the cat by Huntington and McClure.


In the 15 mm Harvard embryo (fig. 11) the caudal end of each metanephros rests upon the umbilical. artery (A.Umb.), and its cranial end lies lateral to the renal collar (Anast.Subc.6'prc.), so that the metancphros occupies a somewhat oblique position with respect to the postrenal division of the inferior vena cava and to its homologue on the left side of the body. As stated above, the right metanephros is encircled by a venous ring, formed laterally by a portion of the posterior cardinal vein (I-’c.2), which is absent on the left side where no Venous ring is present.


In the 16-mm embryo the cranial end of each metanephros still occupies its former position, lateral to the renal collar and at the same level. Its caudal end, however, has changed its position, so that it no lon.ger rests upon the umbilical artery. This change has been brought about by a lateral and slight dorsal rotation of its caudal end, so that along its entire extent the metanephros now lies lateral to the main caval channels in the lumbar region. The more lateral and dorsal position now occupied by the permanent kidneys is one which makes possible their so-called cranial migration, associated possibly with an unequal growth and extension of Vessels in the lumbar region, to a position where the hilum of each kidney finally lies opposite the renal collar, the level at which the renal veins arise. This lateral and dorsal rotation of the caudal end of the metanephros has been ascribed as resulting from the loss of the lateral component of the perimetanephric (periureteric) venous ring (Pc.2, fig. 12), whose presence would appear to prevent such a rotation. VVhether the loss of this portion of the ring is the immediate cause by which the rotation is initiated is, however, still open to question, as, on the left side of the 15-mm Harvard embryo, where this component of the venous ring is absent (Pc.2, fig. 9), no indication of a rotation is evident. It appears to the writers that the details of the process involved in the change in position made by the permanent kidneysiare still open to further investigation.


22 mm Human Embryo

Embryological Collection of the College of Physicians and Surgeons (P And S) of Columbia University, No. 1090. (figs. 14 And 15)


We have chosen this 22-mm embryo as the next stage of development to be considered, because it clearly foreshadows the majority of conditions found in the adult and explains the manner in which these have been brought about by a further transformation of the venous plan observed in the 16-mm embryo. A detailed description of the 18-mm embryo of the Harvard Collection (no. 1913) and of the 19-mm embryo of the Cornell Collection was therefore deemed unnecessary.


Among the prominent features illustrated by this embryo are a circumaortic venous ring, known as the renal collar, at about the level of the intersubcardinal anastomosis, and a straightening of the postrenal division of the inferior vena cava and of its homologue on the left side, so that these vessels now lie more lateral to the aorta. Also, an elongation of both caval veins has taken place, and it seems quite probable that an unequal growth of the caval vei11s in the lumbar region may be associated with the more cranial position now occupied by the permanent kidneys. A similar straightening and elongation of the main caval channels had also been accomplished in the 18-mm Harvard embryo, and it would be interesting to study a more closely graded series of stages between this and the 16 mm embryo in relation to the change in position made by the permanent kidneys.


In the 22-mm embryo the postrenal division of the inferior Vena cava on the right side (Sprc.Dcxt.—P.Sprc.) has increased greatly in size and its homologue on the left side (Sprc.Sm.) is a rather insignificant but still independent vessel. The iliac anastomosis (Ana3t.Il.Pc.), also has increased in size, especially in a caudal direction, and has shifted its position to the right side, so that now it lies more nearly in a direct line with the right cava and forms its direct caudal continuation. As a result of this change, blood from the lower limb of the left side now finds the most direct course to the heart through the right inferior vena cava, which has finally acquired its adult relations to the aorta.


As stated above, an important feature observed in this embryo is the presence in its typical form, at about the level of the intersubcardinal anastomosis, of the complete circumaortic venous ring which in the cat has been designated by Huntington and McClure as the renal collar. For details of the development of the renal collar in the cat, the reader is referred to figures 8 to 12, inclusive, in their publication.


The renal collar in the 22-mm embryo can best be observed in figure 15 of the reconstruction, as it was found impossible to represent its ring-like character in diagram (fig. 14) without drawing it in perspective—a method which was not found suitable for illustrating diagrammatically the transformations of the veins. As shown in figure 15, the ventral portion of the renal collar is formed by thecaudal end of the pars subcardinalis of the inferior Vena cava (P.Subc.) and by the intersubcardinal anastomosis (Anast.Int.Subc.); the lateral portions by the right and the left subcardino-supracardinal anastomoses (Anast.S~ubc.Sprc.,I)ext. and Sin.); the dorsal portion by the supracardinal veins and‘ the anastomoses formed between the latter dorsalto the aorta.


While in the 18- and 22-mm embryos blood is still directed from the lumbar region to the prcrenal division of the inferior vena cava through both sides of the renal collar, in the 22-mm embryo the pathway on the right side is of the two the more important. At a later stage the left side of the renal collar is completely lost so that blood is then directed to the prerenal division of the cava elitirely through the right side of the renal collar. As we have shown, this portion of the renal collar l1as been derived from the subcardino—supra— cardinal anastomosis of the right side (Anast.Subc.Sprc. Dexzfl), and in man, as in the cat, constitutes the pars renalis of the embryonic inferior vena cava.


McClure1925 fig14.jpg

Fig. 14 Diagram of the venous system of a 22-mm human embryo of the Embryological Collection of the College of Physicians and Surgeons (Columbia University), no. 1090.


McClure1925 fig15.jpg

Fig. 15 Reconstruction of the venous system of a 22-mm human embryo of the Embryological Collection of the College of Physicians and Surgeons (Columbia University), no. 1090.


In the lumbar region of the 22 mm embryo, anastomoses are present between the caval veins (Anast.I~nt.Sprc., fig. 15) and lie dorsal to the aorta. They are, however, by no means so prominently developed as in the cat and, on account of the continued independence of the left caval vein (Spr0.Sm.) in all the stages of man thus far examined by us, we are bound to conclude that the left caval vein (Sprcn) does not, as in the cat, partly contribute to the formation of the adult inferior vena cava in the lumbar region (figs. 6 and 7 in Huntington and McC1ure’s publication).


The lumbar supracardinal veins (Sprca), immediately cranial to the renal collar, are not of large size in the 22 mm embryo, and it is difficult to determine whether or not a connection exists between them and the more cranially situated supracardinal veins in the azygos region (Sprc.Az.).


It may be mentioned here that the left innominate vein (Im1om.Sm., fig. 14) was by us first observed in the 22 mm embryo. It has previously been figured by Keibel and Mall, however, as present in a 20 mm embryo of the Mall Collection.


In the 22 mm embryo we were for the first time able to determine the presence and follow the course of the definite sex veins (Vv. spermaticae mtemae). In younger embryos veins from the gonads had been observed apparently opening into small veins draining the mesonephros, but definite channels wcre followed with difliculty. It is now possible to observe and to follow with accuracy a vein, arising in each gonad (T/7.8.1., figs. 14 and 15), which courses craniad and, in common with veins draining the mesonephros, joins the lumbar subcardinal, so that the cranial portion of each subcardinal, caudal to the intersubcardinal anastomosis, now functions as the definite sex vein. Details of the relations of the sex veins to the mesonephric venous drainage and to the subcardinal veins are clearly shown in figure 15 of the reconstruction.


In the cat, in addition to the subcardinal, a definite portion of the posterior cardinal vein enters into the formation of the sex vein in the adult (S.V. in figs. 6 and 7 in Huntington and McClure’s publication). The absence in the sex vein of man of a definite portion of the posterior cardinal is plainly due to the early degeneration of the latter in the course of ontogenetic development. The similarity in composition of the sex veins in human embryos with those of the sauropsida is interesting, since in both cases they are derived from the subcardinal veins. This finds its explanation in the circumstance that the embryonic subcardinal drainage system is inseparably connected with that of the mesonephroi which drain into the posterior cardinal veins; the ultimate drainage plan of the gonads of Vertebrates in general therefore depends upon the fate of the posterior cardinal veins in the course of ontogenetic development.


The metanephroi have completed their so-called cranial migration, and permanent renal veins have been formed which receive blood from the kidneys. Each kidney is an organ of relatively large size and, with its hilum at the level of the renal collar, now occupies a position approximately between the level of origin of the umbilical arteries and a point slightly caudal to the level of origin of the coeliac axis. The ureters run caudad and lie dorsal to the sex veins. The relations which the ureters hold to the veins in general in this embryo are indicated by the long arrows X and Y in figure 14.


Two renal veins are present on each side of the body, one (Real) opening into the lateral portion of the renal collar and the other (Renll), more dorsally situated, into the cranial extension in this region of the lumbar supracardinal vein. In the cat the more dorsally situated of the two embryonic renal veins connects directly with the lateral por— tion of the renal collar. Only one 22-mm human embryo was studied; if a larger number of embryos of this age had been examined, a similar condition might occasionally be found to be present in man. "


With the exception of the presence of an inferior vena cava on the left side of the body and of a few minor changes which result when the latter has disappeared, the conditions observed in this 22-mm embryo represent essentially those found in the adult. Before proceeding to a consideration of the final transformations which lead to the conditions found in the adult, we may first consider the conditions observed in a 45-mm human embryo.

45 mm Human Embryo

Harvard Embryological Collection, No. 2123. (fig. 16)

Upon examining this embryo which had been secured for the study of a stage more nearly approaching that of the adult than the 22-mm embryo of the P and S Collection, it was evident we were in possession of one in which the postrenal division of the inferior vena cava had not been developed in a typical manner. We have accepted the atypical condition presented by this embryo as fortunate, since it clearly emphasizes-the existence of a potential modification of the embryonic venous system which is often carried into the adult. '


The prerenal division of the inferior vena cava is entirely typical in its formation and relations and therefore needs no further mention. The principal feature illustrated by this embryo is the presence, at this relatively late stage, of two inferior caval veins in the lumbar region, the principal and larger one being located on the left instead of the right side of the aorta. As shown in figure 16, the pars subcardi nalis of the inferior vena cava (P.S'ubc.-Subc.Dea=t.) makes a sharp bend to the left in the region of the intersubcardinal anastomosis (44.'”'a8t.I’nt.AS'“bC.) and is then continued caudad by the main caval channel which lies on the left of the aorta (Sprc.S-in.-P.Sp«re.), so that in this case the intersubcardinal anastomosis (An-ast.Int.Subc.) and the left side of the renal collar (P.Ren.) enter into the composition of the main caval channel. A much smaller but typically formed inferior vena cava is also present o11 the right side of the aorta (S79rc.I)em2‘.) and conneetswith the prerenal division of the inferior vena eaya through the right side of the renal collar, which is much less developed than the left side.


McClure1925 fig16.jpg

Fig. 16 Reconstruction of the venous system of a 45 mm human embryo of the Harvard Embryologieal Collection, no. 2128. Atypical condition of inferior vena cava (Type BC); persistenee of both supracardinal veins in lumbar region, the vein of the left side being the main channel.


Only one renal vein is now found on each side of the body and, as in the eat, it is formed by the confluence of two main tributaries to form a single Vessel which connects with the lateral portion of the renal collar (Ren.l,I)ea7t. and S'l77,.). It is clear that the presence in the adult of two renal Veins on each side of the body could be explained by the persistence of the two embryonic renal Veins as found in the 22-mm, embryo of the P and S (lolleetion (Reu.I and Re~1z».II, figs. 374 14 and 15). It is also true that, should the bifurcation of each renal vein extend back to its connection with the renal collar, four renal veins might be found in the adult on each side of the body. In fact, a still further multiplicity of renal veins might result by a secondary bifurcation of the two main tributaries of each embryonic renal vein.


As stated above, each sex vein (V.S.I.,Dext. and Sin.) has been derived from the cranial portion of the lumbar subcardinal vein and a newly formed vessel connecting the gonad with the subcardinal through the mesonephric venous drainage. The sex Veins (VV. spermaticae internae) have now straightened their course and extend directly from the sex glands to the inferior vena cava. In the case of the atypical embryo in question, each sex vein still occupies the same relative position with respect to the intersubcardinal anastomosis (Amtst/.Imf.Subc.) and to the derivatives of the subcardinal Veins cranial to this anastomosis (P.Subc. and Adr.Sm.) as at an earlier stage of development (figs. 5, 7, 9, 12, and 14:). The double connection made by the right sex vein (V.S.I.,Dext.) with the cava in the 45-mm embryo represents a rather common atypical condition found in the adult, in which the connection of the sex vein with the cava is double. This atypical arrangement of the sex vein in the adult apparently finds its explanation in the circumstance that the sex vein of subcardinal origin in earlier stages of development (figs. 14 and 15) makes a double connection with the cava and that both of these connections have been retained in the adult.


A median channel (Sprc.X, fig. 16) has been formed between the supracardinal veins from the intersupracardinal anastomoses and can be followed well into the thoracic region. As this vessel has been found to persist in the adult as a variant condition, its presence in the embryo may possibly be a regular and constant feature. A further examination of more advanced stages than have been examined by us would be necessary to determine this question?

  • In a personal communication to the senior author in 1921, Dr. Ivan Wallin, of the University of Colorado, described the presence of this median azygos vessel as occurring in an adult man (cadaver no. 22).


The continued development of this 45-mm embryo might have resulted in an adult variant condition in which both caval veins persisted in the lumbar region, but, in any event, one may reasonably infer that the left cava would have remained the more important Vessel of the two. The independent character of the right inferior vena cava in the 45 mm embryo further emphasizes the fact that the postrenal division of the inferior vena cava in man is not, as in the cat, formed, in part, by a fusion of the lumbar supracardinal veins.


We have not been able in a normal embryo to determine at what age the left inferior vena cava is lost. It is, however, probably the last of the embryonic veins to disappear. This might account for its more or less frequent retention in the adult in connection with the cava of the right side.


The reader is now referred to figure 17, which illustrates the manner in which we believe the normal conditions are established in the adult as the result of a further and final modification of the embryonic venous plan.


By the loss of the inferior cava on the left side (0, fig. 17), blood is necessarily directed from the iliac anastomosis (Anast.Il.Pc.) to the prerenal division of the inferior vena cava exclusively through the large caval vessel (B, fig. 17 ) on the right side. The inferior vena cava, along its entire extent as usually found in the adult, is therefore formed.


On the left side, only one of the two embryonic renal veins (Renl) is usually retained and opens into the left side of the renal collar which, together with the intersubcardinal anastomosis, into which the left sex vein (V.S.I.,Sin.) and the left adrenal vein (Adr.Sz'n.) open, enters into the composition of the left renal vein. If the dorsal portion of the renal collar should be retained, the left renal vein would then connect with the cava of the right side dorsal as well as ventral to the aorta. This dorsal portion of the renal collar ordinarily disappears, however, and with it probably the more dorsally situated of the two embryonic renal veins (Renll, fig. 14), so that on the left side of the adult there is present only one renal Vein (Ren.I,S'in..) which joins the inferior Vena cava ventral to the aorta, and receives the left sex Vein and the left adrenal vein.


Also, on the right side only one of the two embryonic renal veins is usually retained—-probably the more ventrally situated of the two (Ren.I.,Deact.). The loss of the dorsal renal vein (Refill, fig. 14) seems to be associated, as on the left side, with a degeneration of the dorsal portion of the renal collar, near which this vein connects with the main caval channel.


McClure1925 fig17.jpg

Fig. 17 Diagram of the venous system of adult man.


In the embryo the sex vein of each side has a double connection with the main caval channel (fiig. 14), so that in the adult either one or both of these connections may be retained. As the right sex vein ordinarily joins the cava somewhat caudal to the right renal vein, the more caudal of these two embryonic connections is probably the one retained in the adult.

On the Atypical Conditions of the Inferior Vena Cava as found in Adult Man

A detailed knowledge of the development of the veins is in itself a matter of considerable interest; the special importance and significance of the study, however, lies in the fact that it enables us to interpret the atypical conditions often found in adult man, as well as to predict the forms in which atypical conditions are most likely to appear in the human body.


Huntington and McClure (’20) have published a composite diagram of the embryonic veins in the cat. This diagram is reproduced here in figure 18. By means of this diagram one is able at a glance to determine in any particular instance which of the embryonic veins during the course of ontogenetic development have been retained and have entered into the composition of the venous system of the adult cat. They have described fifteen different types of inferior venae cavae occurring potentially in the lumbar region, and all but three of these (types ABD, ABCD, and BOD) have been found in the adult cat by them or by others. These fifteen types are established by the combinations which exist in the lumbar region between the right (A) and left posterior cardinal (D) and the right (B) and left supracardinal (C) veins (fig. 18). The persistence in the adult of any one of these four veins,


Or any combination among them, constitutes 21 distinct and definite type of caval vein in its postrenal division. These types are as follows (fig. 18) :

  1. Type A, persistence of right posterior cardinal Vein (A).
  2. Type AB, persistence of right posterior cardinal (A) and right supracardinal (B) Veins. Right periureteric venous ring.
  3. Type ABC, persistence of right posterior cardinal (A), right supracardinal (B), and left supracardinal (C) veins. Right periureteric Venous ring. D
  4. Type ABCD, persistence of right posterior cardinal (A), right supracardinal (B), left supracardinal (C), and left posterior cardinal (D) Veins. Right and left periureteric venous rings.
  5. Type ABD, persistence of right posterior cardinal (A), right supracardinal (B), and left posterior cardinal (D) Veins. Right periureteric Venous ring.
  6. Type AC, persistence of right posterior cardinal (A) and left supracardinal (C) veins. 1
  7. Type ACD, persistence of right posterior cardinal (A), left supracardinal (C), and left posterior cardinal (D) Veins. Left periureteric Venous ring.
  8. Type AD, persistence of right (A) and left posterior cardinal (D) veins.
  9. Type B, persistence of right supracardinal Vein (B). Normal type of inferior vena cava in adult cat and man (fig. 17).
  10. Type BC, persistence of right (B) and left supracardinal ((7) veins (fig. 16).
  11. Type BCD, persistence of right (B) and left supracardinal (C), and left posterior-cardinal (D) Veins. Left periureteric Venous ring.
  12. Type BD, persistence of right supracardinal (B) and left posterior cardinal (D) Veins.
  13. Type C, persistence of left supracardinal vein (0).
  14. Type CD, persistence of left supracardinal (C) and left posterior cardinal (D) Veins. Left periureteric Venous ring.
  15. Type D, persistence of left posterior cardinal Vein (D).


McClure1925 fig18.jpg

Fig. 18 Composite diagram of the embryonic veins of the domestic cat (Felis <lo1nes’ri(~:2).


In the preceding pages it has been shown that, in man as in the cat, we have the same embryonic plan of the Venous system and the same embryonic components entering into the formation of the adult inferior Vena cava. Minor differences are met with, however, in the relative functional value of the posterior cardinal veins, which, especially the vein of the left side, undergo atrophy at a relatively much earlier stage of development in man than in the cat. Since the groundplan of the embryonic venous system is fundamentally the same in man as in the eat, it would therefore be possible for any one of these fifteen types of caval Veins to persist in adult man. This is made evident by comparing the veins designated by the letters A,B,C, and D in figures 7, 9, 12, 14, and 17 of man with the corresponding veins in figure 18 of the cat. The relatively early disappearance of the posterior cardinal veins (A and D in all figures) in the human embryo makes it highly improbable, however, that variant types of caval veins in which the posterior cardinals are involved (types A, AB, ABC’, ABCD, ABD, AC, ACD, AD, BOD, BD, OD, and D) would be found as frequently in adult man as in the cat, and such has actually been found to be the case. A comprehensive survey of the literature made by Huntington and McClure has shown that, with exception of type A, not a single case of an atypical inferior vena cava has thus far been described, in which a posterior cardinal vein has persisted in adult man. One can easily determine when a posterior cardinal vein persists in the adult by the relations which the ureter invariably bears to the veins. These relations are shown in figure 18, and are indicated by the long arrows X and Y in this and in the other diagrams. Literature on the subject has shown that the atypical forms of the inferior vena cava most commonly found in adult man are of types BC and C, in which only the supracardinal veins in the lumbar region are concerned. So far as we know, sixty-four cases of type BC and only eighteen of type C have thus far been described. VVhile these figures in no way indicate the number of cases which have actually been observed, they would seem to indicate that type BC is the more common of the two. As shown in the 45 mm embryo (fig. 16), the retention until a relatively late stage of the two inferior caval veins may possibly be associated with the more frequent occurrence in the adult of type


In addition to those mentioned above, another atypical form of inferior vena cava observed both in the adult cat and in man is one in which the prerenaldivision of the inferior Vena cava is completely wanting and has been replaced in the thoracic region by the supracardinal (azygos) veins. An inferior Vena cava of this character represents a condition in which the embryonic supracardinal veins have retained their continuity in the lumbar and thoracic regions, as shown in figures 12 and 18, and, in thoracic region, these constitute in the adult the direct and only cranial continuation of the postrenal division of the inferior caval vein. So far as at present determined, the literature has thus far described thirty-five examples of this atypical form of cava as occurring in adult man. The chances that in the adult the thoracic supracardinal veins of the embryo would persist in the manner described, would appear to be potentially the same in man as in the cat.


Cases in which the renal collar of the embryo has been retainedin adult man have been found; also, there have been observed in both cat and man cases in which the ventral circumference of the circumumbilical venous rings (C.C'.) have been retained in the adult (Huntington and McClure, ’20, pp. 17-18).

It has been observed by Huntington and McClure that in the cat the subcardinal veins in the lumbar region anastomose with each other at intervals in the midline. This, they believe, may account for the occasional presence in the adult of a connection between the sex veins of opposite sides. As corresponding multiple intersubcardinal anastomoses have not so far been observed in the embryos of man, it is evident that similar connections cannot be carried into the adult stage.

Summary

In man, as in the cat, the inferior vena cava is composed of four embryonic subdivisions: Pars hepatica, pars subcardinalis, pars renalis, and pars supracardinalis. While the development of the cava is essentially the same in both cases, nevertheless minor differences are found in the relative functional role played by certain of the embryonic veins during the course of ontogeny.


In man the posterior cardinals disappear at a relatively early stage, and the venous drainage of the mesonephroi in the lumbar region is then transferred to the lumbar subcardinal veins. The lumbar subcardinal veins which drain the gonads retain their independence and individuality throughout all stages of development and enter directly into the formation of the sex veins in the adult.


In the cat, on the other hand, the posterior cardinal veins play an important functional role until a relatively late stage and continue to receive blood from the mesonephroi during all embryonic stages. The lumbar subcardinal veins which, as in man, originally drain the gonads, practically fuse with the posterior cardinals, and so soon lose their original independence and individuality. The gonad drainage is thereby shifted to the posterior cardinals which form a definite portion of the sex veins in the adult cat.


The relatively early degeneration of the posterior cardinal veins in the embryo of man, as compared with that of the cat, is undoubtedly associated with the fact that while an atypical condition of the venous system in which the posterior cardinals are concerned is rarely found in adult man, this is of frequent occurrence in the adult cat.

Literature Cited

HOCHSTEDTER, F. 1892 Beitrtige zur Entwickelungsgesehichte des Venensysterns der Amnioten. 2. Reptilien (Tropidonotus, Lacerta). Morpholog. Jahrb., Bd. 19.

1893 Beitréige zur Entwickelungsgeschichte des Venensystems der Amnioten. 3. Singer. Morpholog. Jal1rb., Bd. 20.

HUNTINGT0N, G. S., AND MCCLURE, C. F. W. 1907 Development of the postcava and tributaries in the domestic cat. Proc. Ass. Amer. Anat., Anat. Rec., no. 3.

1920 The development of the veins in the domestic cat (Felis doincstica) 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. 20.

Lewis FT. The development of the vena cava inferior. (1902) Amer. J Anat. 1(3): 229-244.

MILLER, A. M. 1903 The development of the postcaval vein in birds. Am. Jour. Annt., vol. 2.

McCLURE, C. F. W. 1906 A contribution to the anatomy and development of the venous system of Didelphys marsupialis (L.). Part 2. Development. Am. Jour. Anat., vol. 5.

ZUMSTEIN, J. 1896 Zur Anatomie und Entwickelung des Venensystems des Menschen. Anut. Hefte, Bd. 6.

Figures



Cite this page: Hill, M.A. (2024, March 19) Embryology Paper - The development of the vena cava inferior in man (1925). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_development_of_the_vena_cava_inferior_in_man_(1925)

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