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Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia.

XVIII. Development of Blood, Vascular System and Spleen: Introduction | Origin of the Angioblast and Development of the Blood | Development of the Heart | The Development of the Vascular System | General | Special Development of the Blood-vessels | Origin of the Blood-vascular System | Blood-vascular System in Series of Human Embryos | Arteries | Veins | Development of the Lymphatic System | Development of the Spleen
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D. The Development of the Veins

Evans HM. The development of the vascular system. In Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia. pp570-708.

Herbert McLean Evans
Herbert McLean Evans (1882—1971)

By Herbert M. Evans. Johns Hopkins University, Baltimore.

  1. The venous types.
  2. The ground-plan of the young venous system.
  3. Transformations of the vv. umbilicales et vitelline.
  4. Transformations of the vv. cardinales anteriores.
  5. Transformations of the w. cardinales posteriores.
  6. The development of the veins of the body walls.
  7. The development of the veins of the extremities.

1. The Venous Types

In the adult, as has been recognized for a long time, the veins tend everywhere to follow the arteries, — i.e., the majority of the veins are w. comites. In the embryo, however, it is possible to satisfy one's self that this is not the primary arrangement, for. if one studies carefully the developing vessels in any area, it will be seen that the earliest arterial and venous trunks are separated from one another so as to stand in reciprocal relation as regards the general capillary bed. Should this primary separation of arteries and veins be perpetuated as the vascular trunks continue to grow, we have the plan which obtains, for instance, in the circulation of the- brain or lung, where larger arterial and venous vessels instead of coursing together are arranged so as to stand opposite one another. As a rule, however, as development proceeds the main vascular stems are found coursing together, — i.e., the veins are true w. comites. We have to recognize, then, tivo types of veins, primary and secondary veins, primary veins standing opposite or alternating with the arteries and trunks, secondary ones coursing in company with the corresponding arteries. 70 Venae comites, which are, then, always later formations, may arise either as a result of shifting of primary trunks in growth or entirely de novo. 11 Splendid examples of the persistence of primary veins are furnished by the great subcutaneous veins of the limbs and trunk (v. basilica, v. saphena, v. thoraco-epigastrica). These are in fact remains of the early border veins of the extremities and of very early body wall trunks and it may hence appear more reasonable why they possess no corresponding accompanying arteries.

2. The Ground Plan of the Young Vexous System

If now one turns to the details of the developing venous system in man, it will be recalled that the remarkable precocious development of the chorionic circulation gives us the vv. umbilicales at stages much earlier than obtain in the mammalia generally. In embryos of 6 somites (N.T. 3) we can also trace clearly the vv. vitellines, and it can be seen that in their terminal portions the umbilical veins join the heart by receiving the vitelline veins and coursing now as a common vitello-umbilical trunk. 12 At the margins of the anterior intestinal portal, this vessel turns inward, courses in the mesial wall of the pleuropericardial passage, and in the mesodermic tissue ventral to the foregut anastomoses with its fellow of the opposite side to constitute the sinus venosus. The latter is at first situated in front of the first somite (Mall embryo 391, with seven somites), but in the fifteen somite embryo (Graf Spee No. 52) is opposite the body of the first somite, and in the twenty- three somite embryo (N.T. 7) is opposite that of the sixth (Thompson, 1908). In this last stage there open into the sinus the anterior and posterior cardinal veins by means of a ductus Cuvieri, but earlier, when the sinus lies more crarfialward, the anterior cardinal vein joins the common vitello-umbilical vein (embryo of fifteen somites). The intermediate stages are not known in man.

70 Even though their peripheral portions, of course, always exhibit a primary separation from the arteries.

71 The primary circulation schema and the secondary birth of venae comites may be seen beautifully in such an expanded flat area as the area vasculosa of the chick (cf. Popoff), but no less clearly, for example, in the extremities, where the primary border vein drains all the blood from the central artery, whereas secondarily venae comites arise (Hochstetter, 1891).

2 This common vitello-umbilical vein of man corresponds really to the end portion of the vitelline veins of other early mammalian embryos in which always umbilical veins secondarily appear later (e.g., rabbits).

At twenty-three somites, then, we have present the four pairs of veins (the vv. cardinales anteriores et posteriores, the vv. umbilicales, and the w. vitelline), which form an entirely symmetrical venous ground-plan, characteristic not only for man but for all the vertebrates. This ground-plan of the venous system remains in embryos which are approximately a centimetre long, and its existence in man has been known to us since the classical descriptions of His (1880 to 1885).

It will be convenient to study the development of the adult venous tree as a modification of each of these primitive systems. The proximal ends of the umbilical and vitelline veins enter into special relations with one another in the region of the liver, and with the further growth of the liver bud are converted into the two venous trees of that organ, the vv. hepaticae and vv. porta?. On account of the early inauguration of these changes, they may be described first.

3. The Transformation of the Umbilical And Vitelline Veins

Mention has already been made of the fact that the vitelline veins are first interrupted in their course to the sinus venosus by the growth of the liver bud, which in embryos from three millimetres on in length, begins to cause the interposition of many smaller vessels (sinusoids of Minot) in the venous current through the liver. The early stages in this process can be seen in the figures supplied us by His (Figs. 425 and 426), where both vitellines have as yet a fairly direct path through the liver region and open on either side into the sinus venosus. Very soon, however, the left v. omphalomesenterica is more effectively cut up into nourishing liver capillaries (sinusoids), although these still drain into the left horn of the sinus venosus by way of the old opening there of the original vein, which hence constitutes a primitive v. hepatica sinistra (Fig. 456).

This persists as late as in embryos of 7 mm. (Elze).

The umbilical veins next gain connections with the liver sinusoids and eventually lose completely their early superficial course in the region between liver and heart, a fact first noted by H. Rathke (1838). 73 The umbilical blood is now poured into the liver channels, the largest of which is the old direct path of the right omphalomesenteric to the corresponding horn of the sinus venosus. In the mean time the two vitelline veins have anastomosed with each other by cross connections, which go, first ventral, then dorsal, and again ventral, to the gut tube and so form two venous rings around the duodenum, as may be seen from Fig. 456. 74 The middle or dorsal of these anastomoses receives the vein from the intestine, the true mesenteric vein.

Cited after His, Anat. Mensch. Embryonen III, S. 210 (1885).

His pointed out that the usual fate of these venous rings involved always the atrophy of certain limbs and the persistence of others in such a way that an S-shaped course is now described by a common vitelline trunk in reaching the liver. It is important to note that during this time the left umbilical vein has effected a direct connection with the cranial venous ring and that the right umbilical atrophies. The right vitelline vein also disappears, so that by the time the embryo is 7 millimetres in length the main source of blood for the liver comes from the left vitelline and left umbilical veins. 75 The liver end of the former vessel is the old S-shaped common vitelline trunk, and where it becomes dorsal to the gut, consequently the place corresponding to the early dorsal venous anastomosis, — the middle one of the three, — it receives the 74 The researches of Hochstetter make it probable that these venous rings (first seen by His in the human embryo) are of very general occurrence among the mammalia.


Fig. 456. — Schema of the liver circulation in a human embryo 4.9 mm. long (NT. 14). (After Ingalls, 1907.

i5 The umbilicalis dextra still connects with the liver sinusoids in the 7 mm. embryo (Elze).

mesenteric vein. Somewhat further headward and after it has turned around the right side of the gut to become ventral to it, and at a place corresponding to the former cranial venous ring, this, now the omphalomesenteric trunk, receives the left umbilical vein. For a time the chief channel for all this blood through the liver is the intrahepatic course of the former right vitelline vein (Mall) (Fig. 458). Soon the development of an anastomosis (already indicated in Fig. 456) enables the vena hepatica sinistra to lead its blood also into the right end of the sinus venosus, near the opening of the right vitelline trunk (secondary v. hepatica sinistra), while the former multiple afferents of the left omphalo

Venae revehentes

Ductus venosus Arantii Pane. d. Venae revehentes

Cranial end of the v. umbiliealisdextra .

Stomach - -_

Vense advehentes

Ductus choledochus V. umbilicalis dext

Cranial end of the v. umbilicalis sinistra

_,.-^g ^---- Vena? advehentes

Li ver

V. umbilicalis sinistra

Obliterated part of Duo- V. ntellina V. vitellina An. v. c. Obliterated part of the venous ring denum dextra sinistra the %-enous ring Fig. 457. — Schema of the liver circulation in the human embryo at a later stage than that shown in Fig. 456. (After His, from Marshall.) Pane, d., pancreas dorsale; An. v. c, annulus venosus caudalis.

mesenteric into the left lobe of the liver are now reduced to a single larger supplying trunk, the ramus angularis (Mall).

When, with the growth of the right lobe of the liver, the intrahepatic course of the right vitelline becomes shifted so as to constitute a somewhat circuitous route, a new direct one to the sinus venosus is formed; this is the ductus venosus Arantii. Mall's researches show that the former intrahepatic course of the right vitelline does not completely atrophy without a trace, but leaves representatives in the form of its end, which drains into the sinus venosus, and its first portion, which leaves the umbilical vein, for these are now incorporated as parts of the supplying (portal) and draining (hepatic) systems of the liver, and become respectively the ramus dexter vena? hepatica? and the ramus arcuatus (et descendens) vena? portae. At this stage, then, we have for both of

flit- two main divisions or Lobes of the liver, porta] or supplying and hepatic or draining trunks; on the left, the ramus angularis venas portae, the blood from which is drained into the ramus sinistra venae hepaticae, on the right, the ramus arcuatus of the portal vein, opposite to which stands the ramus dexter of the hepatic (Mall) Fig. 459).

In an embryo 11 mm. long two trunks have been added to both the supplying and draining systems, and four units or lobes may be described as being present. To the portal system have been added the right and left arborizations of the recessus nmbilicalis (Eex, 1888), to the hepatic the ramus medius and vena cava inferior (Fig. 460). Xowthe middle and left hepatic veins both

I io ~< inidiagrarnmatie reconstruction of the veins of the liver of a human embryo 5 mm. long, Mall No. 80. ) (After Mall, 1906.) L., liver; u. v., umbilical vein; v. o. m., right omphalomesenteric vein; r.h.s., ramus hepaticus sinister; r. u., reces3us umbilicalis; r. a., ramus angularis; m., mesenteric vein; /., intestine.

Fig. 159. — Semidiagxammatic reconstruction of the vein?- of the liver of a human embryo 7 mm. long, Mall Xo. i. (After Mall, 1906.) /...liver: u. v., umbilical vein; m., mesenteric vein; r.u., recessus umbilicalis; d. v. ductus venosus; r. a.,. ramus arcuatus; r.h. </., ramus hepaticus dexter; r. h. «., ramus hepaticus sinister.

divide, and consequently by the stage of 26 millimetres we find six collecting trunk.-, the upper and the lower right hepatic (the latter a branch of the inferior cava), the right and left media, and the ii] 'per and lower left hepatics. Correspondingly six supplying trunks exist, for the right portal branch splits into a ramus ascendens as well as ramus dexter, and, in addition to the ramus angularis, we have also the left arborization of the recessus umbilicalis and two other prominent brandies of this trunk, one of which may be identified as it- right arborization (Fig. 461). Mall pointed out that these six primary lobules of the liver correspond with the six lobes to be recognized in the morphology of the adult mammalian liver (Bex).

ft ha- been pointed out that at the stage of 4.9 mm. the dorsal anastomosis between the vitelline veins receives the mesenteric vein draining the intestine. After the 8-shaped common vitelline vein is formed out of these anastomoses and after the right vitelline vein lias atrophied, the left vitelline becomes the sole efferent from the yolk sac and receives the mesenteric 'vein at the earlier point of union of the latter with the dorsal anastomosis. Prom here on to the liver then this vein is properly the omphalomesenteric vein, hut in most of its conrse it has been free from the mesentery, crossing the coelome Independently of the latter. On the other hand, the omphalomesenteric artery, which supplies both gut and yolk-sac, courses in the mesentery. The artery is directly trans

. A I-"u;. 160 Reconstruction of the vascular system of the li\i-r of a human embryo 11 mm. long. i Mall No. 109.) I \itiT Mall, 1906.) u. v., umbilical vein; p. v., portal vein; r.a., ramus annularis; r. «., ras umbilicalis; r.d., ramus descendens; r. a., ramus arcuatus (possibly ramus ascendens); r.c, rinht arborisation of the recessus umbilicalis; r. /., left arborisation of the recessus umbilicalis; J. v., ductus venosus; i c, vena cava;, omphalomesenteric vein; r. m., ramus medius; r. 8., ramus sinister.

formed into the superior mesenteric artery, hut its accompanying vein (v. mesenterica superior) is a secondary channel which has arisen to drain the gut wall and it alone, the yolk sac drainage going by way of the former left vitelline vein. Only a small pari of the vitelline vein is incorporated in the vena porta o\' the adult, namely, thai part proximal to where the mesenteric vein is re ceived. 78 " It was Luschka (1863) who first pointed out that the vitelline vein does not persist in the v. mesenterica superior, although tins Is largely true for the corresponding artery. Dexter (1902) mid Lewis (1903) for the eal and pig, and Bonnol and Seevers (1906) in the case "t 1 man, have called specific attention to this Pact.

4. The Transformation of the Anterior Cardinal Veins

The anterior cardinal vein suffers profound modifications, for it and its derivatives come to form the sinuses of the dura while its proximal portion constitutes the great internal jugular trunk of the adult. We have already seen that in human embryos of 15 somites the anterior cardinal or, better, the primitive head vein can be identified from the region of the fore-brain to its opening into the common vitello-umbilical vein opposite the third somite, and that it can be divided into a longer portion lying- in front of the region of the somites and a shorter portion in the segmental

Fig. 461. — Reconstruction of the vascular system of the liver of a human embryo 2-1 mm. long(Mall No. 6.) (After Mall, 1906.) u. v., umbilical vein; v. p., vena portse; r. u., recessus umbilicalis; r. a., ramus arcuatus; r. d., ramus descendens; r. a., ramus angularis; r. c, right arborization of the recessus umbilicalis; r. 1., left arborization of the recessus umbilicalis; v. h., vena hepatica; d. v*, ductus venosus; d. s., vena dextra superior; d. i., vena dextra inferior; m. d., vena media dextra; m. s., vena media sinistra; 8. s., vena sinistra superior; s. i., vena sinistra inferior; v. c, vena cava.

area ; the former portion lies close at the sides of the hind-brain and should be known as the v. capitis medialis (Grosser, 1907) ; the latter is situated more laterally and is the true cardinalis anterior. 77 Both portions of the primitive head vein are in frequent connection with the aorta by means of numerous small direct branches, the v. capitis medialis by means of dorsal presegmental arteries, the true cardinalis anterior by means of the dorsal segmental arteries as well as by direct lateral branches of the aorta. Later all of these aortic offshoots atrophy, and the chief source of the blood drained by the primitive head vein is supplied by the a. carotis interna. When the anlagen of the cranial nerves first appear, they are found lateral to the vena capitis medialis, but in later stages, as Salzer (1895) first showed, the vein is gradually shifted lateral to the nerves by the formation of channels which course on the outer side of the latter, and the v. capitis lateralis thus produced gives us a secondary, wholly lateral, head vein.

77 Grosser first separated these two portions of the primitive head vein, which occur in all vertebrates, and called attention to the fact that only the caudal part is homologous with the posterior cardinal and hence merits the name cardinalis anterior. He remarks that the cardinals are probably especially related to the segmental excretory system and that the anterior cardinal is likely evidence of the former cephalic extent of this.

Fig. 462. — Reconstruction of the veins of the head in a human embryo 9 mm. long.

(After Mall, 1905.)

(Mall No. 163/

The development of vascular sprouts which enable the medial head vein to begin to circumvent the ganglia of the cranial nerves occurs early. In embryos 3 mm. in length (Broman, NT. 11) it has shifted lateral to the acustico-facialis, the otic vesicle, and the glosso-pharyngeus. This position we saw it had retained in the embryo of 4.9 mm. (NT. 14). When the sixth nerve can be identified, it also is medial to the vein. Next the tenth nerve is surrounded by a venous ring ami the lateral path around this nerve chosen, to the elimination of the medial oneSuch a ring around the vagus may be seen in 7 mm. embryos (Fig. 420) or. again. may not be formed when a length of 9 mm . is reached (Fig. 462). Gradually a similar loop forms around the Gasserian ganglion (Fig. 463). From the fifth nerve caudalward to the twelfth, then, the medial head vein has become the v. capitis lateralis.

n The v. capitis medialis iu the region of the fifth nerve is retained to become the sinus cavernosns of the adult (Mall), but otherwise the early medial head vein leaves no trace of its existence. The v. capitis lateralis is entirely without the skull, or, more accurately, leaves the skull with the seventh nerve to empty ts blood into the internal jugular vein, and so it takes no part in the formation of the permanent head sinuses, although its chief tributaries do so, as Mall has shown in the following way. At the stage of which we are speaking, the v. capitis lateralis possesses three main tributaries, the anterior, middle, and posterior cerebral veins respectively (Mall). The first of these drains the eye (v. ophthalmica) and cerebral hemispheres as well as mid-brain; its most cephalic extension conrses on either side of the mid-dorsal line in the region of the fore-brain and constitutes the anlage of the erior sagittal sinus, thus primitively paired. The middle cerebral vein drains the anterior part of the hind-brain (cerebellum) and joins the main trunk between the fifth and seventh nerves. Since the v. capitis lateralis leaves the skull in company with the seventh nerve, it is apparent that through this foramen the venous blood of the fore-brain, mid-brain, and cerebellum is drained. The last tributary of the lateral head vein joins it behind the otic vesicle, leaving the skull through the embryonic jugular foramen (v. eerebralis posterior). This posterior cerebral vein drains the remainder of the hind-brain (medulla) and first portion of the cervical cord. As the anterior cerebral vein extends forward to the top of the cerebrum, so also the posterior cerebral reaches the mid-dorsal region of the hind-brain (Pig. 464).

Fig. 463. — Reconstruction of the veins of the headin a human embryo 11 mm. long.

(After Mall, 1905

Mall No. 109. 1

Now anastomoses develop between these three primitive cerebral veins and the v. capitis lateralis atrophies, so that not only the hind-brain blood but that of the entire brain is drained out through the foramen jugulare, and the old anterior exit with the n. facialis disappears. 78 The anastomoses which develop between these three primitive brain veins begin the changes that convert these to the head sinuses. The blood from the sinus sagittalis superior is no longer returned by way of the anterior cerebral vein, but courses dorsally by means of a new anastomosis which links it to the upper end of the cerebralis media. Very soon, though, an anastomosis is carried still further caudally, so that the blood now enters the posterior cerebral vein, which leaves the skull through the jugular foramen. This last and most important anastomosis forms the original cerebraiis media is probably incorporated to form the superior petrosal sinus, but the inferior petrosal sinus is a later formation. 79 " 1 The v. jugularis externa is a secondary venous channel which in man, as in the mammals generally, appears relatively late (embryo of 16 mm., F. T. Lewis, 1909; see also Schawlowski, 1891). We possess as yet no connected history of the vein for man.

Fig. 464. — The right vena cerebralis posterior (Mall) draining the roof of the hind-brain in a human embryo 11 mm. long. (Mall No. 353.) Injection preparation. (After a sketch kindly placed at my disposal by Mr. Max Broedel.) major portion of the lateral sinus, and in the fetus of 33 mm. is a large channel which has completely supplanted the old v. capitis lateralis. This great channel is gradually shifted backward in later stages by the growth of the cerebral hemispheres. The 78 Salzer and Mall call attention to the fact that in all probability Kolliker mistook this exit of the v. capitis lateralis from the skull as a drainage of the early head by the external jugular vein, and hence thought that he had confirmed Luschka, who believed that this was the case and that only secondarily did the internal jugular drain the brain. Luschka fancied that the foramen jugulare spurium, to which he first called attention, represented this primary exit of the skull drainage. The internal jugular, however, is from the first the only vein of the brain, and this is true also after the skull begins its development. The external jugular vein is an entirely secondary channel much later to develop. It is of interest to note that Hochstetter has shown that in the adult of Echidna the blood of the anterior part of the brain is drained by the persisting part of the v. capitis lateralis, which leaves the skull with the facialis and thereafter joins the internal jugular trunk. In Ornithorhynchus also, as Hochstetter has shown, the same vein exists, but it is only supplementary here to the vein traversing the foramen jugulare.

The reader will find the mention of some stages in the development of this vein in the guinea-pig given by Salzer (1895) and in the bat by Grosser (1901).

We have seen that in early embryos the floor of the branchial region is drained on each side by a vein which originally joinsi the duct of Cuvier but is soon a tributary of the anterior cardinal. 79 " Lewis (1909) has traced this vein in a series of embryos, and believes it can be recognized as the linguo-facial vein of the adult, where it usually belongs to the external jugular trunk. Its transfer from the internal to the external jugular appears after the stage of 16 mm.

The proximal ends of what were originally the anterior cardinal veins do not continue to open into the heart separately, — i.e., by means of two ducts of Cuvier, formed by the union of anterior and posterior cardinal veins on each side. Only the right opening persists, and this is possible by the development of a great anastomosis between the anterior cardinals (Fig. 478) which enables the left vein to conduct all its blood into the right one. The anastomosis becomes the v. anonyma sinistra, 80 and that portion of the right anterior cardinal between the opening of the v. anonyma sinistra and the right subclavian vein is known as the v. anonyma dextra, whereas the lower portion of the right anterior cardinal and the right ductus Cuvieri becomes the vena cava superior. The original portion of the left anterior cardinal below the transverse anastomosis becomes the end portion of the v. hemiazygos accessoria, the remainder of which is constituted by the left posterior cardinal ; of the left ductus Cuvieri only the proximal portion is preserved as the sinus coronarius (Marshall, 1850).

79a Grosser (1907) has shown this to be homologous with the inferior jugular vein of fishes.

79b The reader is referred to the recent study of the development of these veins made by J. Markowski (1911). (Markowski, Ueber die Entwieklung der Sinus durae matris und der Hirnvenen bei mensehliehen Embryonen von 15.5—49 mm. Scheitel-Steiss lange, Bull, de l'Acad. des Sciences de Craeovie, Juillet, 1911.) so Schawlowski (1S91) and Anikiew (1909), from fragmentary observations on human embryos, conclude that veins draining the thymus gland are concerned in the formation of this anastomosis (v. anonyma sinistra).

5. Transformations of the Posterior Cardinal Veins

We have seen that the posterior cardinal veins form two long symmetrical drainage channels which receive dorsally segmental afferents si (vv. intercostales et lumbales) and ventrally many small tributaries from the Wolffian bodies, and that, when the hind limbs develop, their chief afferent — the fibular border vein — also opens into the posterior cardinal.

Gradually, now, two veins arise to assist in the drainage of the mesonephros. These are the w. subcardinales (F. T. Lewis, 1902), and have already been noted in the preceding accounts of several embryos (vide pp. 604, 612). They lie on the ventral surface of the mesonephros on each side, and each of them is not only connected at either end and at many other points with the corresponding posterior cardinal vein, but also joins its fellow of the other side by means of cross anastomoses across the front of the aorta. The latter communications are soon confined to one large connection just below the origin of the a. mesenterica superior and at the level of the future w. renales.

Although for a time the subcardinal veins can only thus be considered accessory and tributary to the posterior cardinals, the right subcardinal acquires another highly important connection headward with the vascular system of the liver (the hepatic half), 82 and it is afterward possible for a great part of the blood from the hind end of the body to stream directly into the heart by means of the common hepatic vein (v. hepatica revehens communis). 83 This connection inaugurates a profound change in the drainage of the legs and lower trunk, the end result of which is the substitution of a single large channel — the vena cava inferior — in place of the earlier multiple and symmetrical veins.

For the details of this change we are indebted mainly to the investigations of F. Hoehstetter and of F. T. Lewis on the rabbit. A complete account for man, founded on a satisfactory series of human embryos, is still lacking. I shall accordingly content myself here with a brief presentation of the essential facts won from other mammalian embryos and of the probable history in man. This is the more justifiable also, since we possess many scattered observations, on such human material as has been at hand, by Hochstetter, Zumstein, and Kollmann, among others.

  • 81 It may again be emphasized that in the beginning the posterior cardinals receive more of the cervical segmental veins than later. These, with the exception of the first, drain into the v. cardinalis posterior, but with the descent of the heart and great vessels, the cervical veins become tributaries of the anterior cardinal.
  • 82 It is of interest to note that Davis (1910) has demonstrated open connections between the subcardinal veins and the portal system in early embryos of the pig, but these reach their maximum and are obliterated before the vena cava is formed.
  • 83 Hoehstetter thus names the trunk passing from the liver to the heart and formed, as we have already seen, from parts of the hepatic, umbilical, and omphalomesenteric veins. It has been pointed out that some of the blood from the lower limbs and tail can stream through the sinusoidal vessels of the Wolffian body and join the vena cava, thus giving us a partial renal-portal system for the mesonephros of mammals. Yet in mammalian embryos we must grant Hochstetter's remarks that the characteristic renal-portal system of Sauropsida is only approached.

Keibel Mall 2 465.jpg

Fig. 465. Sagittal section through a pig embryo 8 mm. long, showing the hepatic and subcardinal capillaries approaching one another to form the vena cava inferior. (After Davis, 1910.)

The exact manner in which the cardinal system is tapped by the hepatic was pointed out by F. T. Lewis (1902) and more recently by D. M. Davis (1910). The latter observer has shown that the capillaries on the ventral surface of the Wolffian body proliferate in a cephalic direction, fusing with capillaries which surround the oesophagus (peri-cesophageal plexus) and which course also on the wall of the stomach. Thus the drainage territory of the subcardinal vein is extended headward. On the right side, beyond the anterior limit of the Wolffian body, this skirmish line of capillaries grows in the connective tissue of the caval mesentery which has also been invaded by hepatic capillaries in advance of liver cells. Soon hepatic and subcardinal capillaries meet and fuse, and for the first time a vascular path is offered from the right subcardinal to the common hepatic vein (Fig. 465). Inasmuch as both subcardinal and cardinal veins are in frequent connection, this new path diverts much of the blood stream of the lower posterior cardinal, which formerly went to Cuvier's duct, through this new channel. Thus in the posterior cardinal veins we may now be said to have two blood streams, for the current in the lower part of both veins turns ventrally into the upper right subcardinal vein by virtue of the great anastomoses between cardinals and subcardinals, whereas in that part of the posterior cardinals above the level of the Wolffian bodies the blood goes upward to the ductus Cuvieri. This leads to a more or less complete separation of the two portions of the posterior cardinal vein. The upper portions of these veins are transformed into the system of the azygos and hemiazygos veins of the adult; the lower portions undergo still other changes. 84 For a while, although disturbed by the migration of the permanent kidneys, 85 they remain quite symmetrical, and so the vena cava appears double in the region below the great anastomosis above mentioned. 86 Eventually, however, only the lower segment of the right posterior cardinal persists to constitute the peripheral segment of the single adult vena cava inferior, for the left vein atrophies 87 in virtue of anastomoses between the two cardinals which enable the right channel to drain satisfactorily all the blood. The chief of these anastomoses (the transverse iliac vein) enables the blood from the left pelvic region, and the left limb to drain practically entirely into the right cardinal. In this way the transverse iliac vein constitutes the tenninal portion of the left common iliac, which has hence a morphological value different from the terminal part of the right v. iliacus communis. 88 Anastomoses also enable the left lumbar veins to be carried across the vertebral column to open into the right lower cardinal (cava), whereas the upper great anastomoses between the cardinals remains as the proximal part of the left adult renal vein. It is only necessary to add that the subcardinal veins below the level of the great transverse anastomoses atrophy, while that portion of the left vein above this level functions as the proximal part of the left adrenal vein. It hence goes into the renal vein (which represents in part the original great trans-anastomoses), rather than into the vena cava directly, as the right adrenal vein does. • The vena cava inferior, then, is a composite vessel, and is formed, from the liver downward, of parts of the following veins : right hepatic vein, connecting vein in the caval mesentery, right upper subcardinal vein, and right lower posterior cardinal.

84 These lower portions of the posterior cardinal veins persist symmetrically in some mammals and so form a vena cava which is double below the level of the vv. renales (Echidna, Edentates, Cetacea).

85 As the anlage of the permanent kidney ascends from the pelvis to its permanent position, it appears to push in between the aorta and the posterior cardinal vein and to displace the latter ventral- and lateralward. A more direct collateral venous path is developed going dorso-medial to either the ureter or the kidney anlage, which may for a time be thus surrounded by a venous ring. (Vide Hochstetter, 1S93; Zumstein, 1887 and 1S90; Grosser, 1901; Lewis, 1902.) 84 An arrangement which may persist in those well-known anomalies in which we have a double cava below the kidneys.

OT Hochstetter states that the lower left cardinal obliterates up to the point of reception of the spermatic (ovarian) vein, and that consequently the end portion of this lower left cardinal is represented in the most proximal part of the left spermatic vein of the adult. The opinion that part of the left cardinal is represented by the ascending lumbar vein (Lewis, Bryce) is disputed by him, on the ground that the latter has a more lateral position. He assigns the origin of this vein to secondary anastomoses which establish a chain between the thoracic and iliac region. It is of interest to note that the atrophy of the left lower cardinal is not the only method by which a single adult cava is produced in the region below the kidneys. In some mammals this is attained apparently by a true fusion of the two cardinals dorsal (Ornithorhynchus) or ventral (most Marsupials) from the aorta (Hochstetter).

  • "Which is probably only the proximal part of the early v. ischiadica.

The upper portions of the posterior cardinal veins are undoubtedly concerned in the formation of the vv. azygos and hemiazygos. 89 Here again, though, we possess as yet no accounts for the embryo of man. The arrangement of the veins in question in the adult shows that normally in further growth an asymmetrical development of these two veins occurs. This, nevertheless, is not

Fig. 466. — Injection of a pig embryo 8 mm. long, showing the extensive system of transverse bodywall tributaries to the umbilical vein. (After Smith, 1909.) V.l.f., vena linguo-facialis; S. r., sinus reuniens; Pars sup. v. r., pars superior v. umbilicalis; m. r., membrana reuniens; v. u. d., vena umbilicalis dextra; V. c. a., v. cardinalis anterior; V. c. p., v. cardinalis posterior.

usually so extreme as is the case, for instance, with the rabbit, where the right vein alone persists. In man, as is well known, the left trunk is only interrupted, for, while the lower portion joins 88 In all accounts hitherto given us, the upper portions of the original posterior cardinal veins have been described as entirely separated from their lower portions by the great deflection of the venous blood current due to the appearance of the inferior cava, and this "separation" occurs at such a level (e.g., the eighth thoracic segment, rabbit) that these upper portions of the posterior cardinals must be subsequently extended to the end of the thoracic region to constitute the a2ygos of the adult. They are, in fact, described as actually "growing down" secondarily. Hochstetter (1903, p. 604) comments on the conditions he found in a 15.5 human embryo, in which the adrenal glands destroyed the symmetry of the posterior the right vein (v. azygos) by means of one or more large cross anastomoses, its upper portion, the so-called v. hemiazygos accessoria, continues to Cuvier's duct. 90 Information on the exact details of the transformations effected in these venous channels in various mammals should be sought in the papers of Hochstetter, Zumstein, Lewis, Grosser, McClure, Gosset, Parker and Tozier, Van Pee, Beddard, Soulie and Bonne.

Fig. 467. — Injection of a pig embryo IS mm. long, showing the superficial body wall veins. (After .Smith, 1909.) Plexus v. e. s., plexus of superficial epigastric vein; V.m.i., v. mammaria interna; Y.t.e-, v. thoraco-epigastrica.

6. The Development of the Veins of the Body Wall

We have seen that in young embryos the body walls are drained into the umbilical vein by an extensive svstem of tributaries. There is no doubt, then, but that we must regard the v. umbilicalis as the primary drainage channel for the body wall. 91 Its domain here is next disputed by the appearance of the v. thoraco-epigastrica? 2 which forms on the lateral body wall just caudal to the arm bud. Proximally, the thoraco-epigastrica unites with the primitive ulnar vein to constitute the v. subclavia, which, as Hochstetter (1891) first showed, at first courses dorsal to the brachial plexus and subclavian artery to enter the v. cardinalis anterior (embryo of 10 mm., F. T. Lewis, 1909), but in slightly

eardinals: "Audi hat dieses Organ (die Nebenniere) das Kopfende der Urniere, welches sich somit schon sehr stark retrahiert hat, so weit lateralwiirts abgedrangt, class ein Zusammenhang der v. azygos und hemiazygos niit don Venen dieses Organs nicht mehr bestehen kann. Der geschilderte Befund lasst bedeutende Zweifel dariiber aufkommen, ob die v. azygos und hemiazygos beim Menschen in ihrer Totalitat als Reste der hinteren Kardinalvenen aufzufassen sein werden." 90 But exceptional cases in which an entirely symmetrical doubled schema ipreserved are by no means uncommon in man, and in some mammals, on the other hand, this is a normal course of development, — e.g., Echidna (Hochstetter).

Fig. 468. — Injection of a pig embryo 15 mm. long, showing symmetrical mid-ventral veins draining the plexus situated in the membrana reuniens over the heart.

older embryos possesses also an opening ventral to these structures, so that in the latter stage (embryo of 11.5 mm., F. T. Lewis, 1909) the a, subclavia and plexus brachialis are enclosed in a venous ring, only the ventral limb of which will persist.

91 Since the complete system of these veins has not yet been figured for human embryos, I present here three figures to show their extent in another mammal (the pig). Miss Smith's figures (Figs. 466, 467) have been secured from injections of living embryos, and I supplement them by a figure to show the plan of mid-ventral drainage (Fig. 468). Here one remarks that the membrana reuniens over the upper portion of the heart territory is drained by two parallel mid-ventral veins which eventually join the v. umbilicalis. (In some instances they also end by branches which sink in directly to the vessels of the liver.) 12 Homologous with Hochstetter's "Seitenrmnpfvene" of the lower vertebrates.

Owing to the fact that at first the lateral body walls greatly exceed in extent the dorsal and ventral surfaces, their chief drainage channels, the vv. thoraco epigdstricce, are the most important body-wall veins until relatively late (embryo of 50 mm). What proportion of the body-wall drainage they still control in an embryo of 35 mm. can be seen from Fig. 473. At this later stage, however, the more ventrally lying veins begin to play a significant role, among which are to be mentioned the superficial epigastrics and the perforating branches of the vv. mammaria internee and inter co stales. In embryos of 50 mm, injections show that the territories of these latter veins have grown very appreciably, yet there do not occur as yet any appreciable anastomoses, such as produce here the great venous plexus well known in the adult (Fig. 472).

7. The Development of the Veins of the Extremity

We lack as yet any thorough-going account of the development of the extremitv veins in man. Nevertheless, the researches of

Fig. 469. — Injected human embryo 11 mm. long, showing some of the chief superficial veins. (From a drawing by Mr. Max Broedel.) (Alall No. 353.1 T.e. v., thoracoepigastric vein; P. c. v., posterior cerebral vein; U- v., umbilical vein.

F. Hochstetter (1891) on the extremity veins of Amniotes and the scattered observations which have been made on the human embryo, together with some others which will be presented here, enable us to outline the essential facts in this field.

The first veins of the limb bud in man, as in other mammals and in the chick, are small direct vessels which drain the early capillary plexus of the limbs into the posterior cardinal and umbilical veins. These venules thus constitute two sets — a dorsal series, which are the tributaries of the posterior cardinal vein,

Fig. 470. — Injected human embryo 20 mm. long, showing some of the chief superficial veins. (Mall No. 349. (After drawings kindly placed at my disposal by Mr. Max Broedel.)

Fig. 471. — Injection showing the thoraco-epigastric and superficial epigastric veins in a human embryo 35 mm. long. (Mall No. 449.) Fig. 472. — The same in an embryo 50 mm. long. (Mall No. 458.) The relative growth of the lower .vein is evident. No anastomoses between the two systems are yet present.

and a 'ventral series, the tributaries of the umbilical vein. Such are the conditions in human embryos under five millimetres in length.

Fig. 473. — Body-wall veins of a human fetus 35 mm. long. (Mall No. 449,) The specimen was secured alive through the kindness of Dr. Thomas Cullen and injected through one of the aa. umbilicales.

But there is soon established in both limbs (in the anterior limb first and later in the posterior) a border vein which surrounds the paddle-like extremity, 93 a vein which Hochstetter has shown to be characteristic for the limb bud of all the amniota. The

93 The observations of Lewis and Grosser have indicated that both radial and tibial border veins are extremely transitory; Grosser, in fact, was not able to find a tibial border vein in the bat ; however, Bardeen figures this clearly in his studv of the leg bud of a 11 mm. human embryo ( Amer. Jour. Anat.. I, 1901. PI. IV, Fig. D, p. 36).

Injections of the limb buds of pig einbryos show that the border vein is constructed out of the peripheral margin of the capillary plexus of the limb.

upper (radial and tibial) portions of these border veins are quite insignificant, but the lower (ulnar and fibular) ones are relatively large 94 and constitute the chief channels of drainage of the extremities. Moreover while the radial and tibial border veins completely atrophy, the ulnar and fibular veins persist, their peripheral portions constituting the basilic and small saphenous veins of the arm and leg respectively. Proximally the ulnar border vein constitutes the definite branchial, axillary, and subclavian vein. For a considerable time this is the only important venous channel in the arm, and, although its proximal portion still functions as the

Figs. 474 and 475. — Reconstructions of the veins of the right arm in two human embryos 10 and 11.5 mm. long respectively. (After F. T. Lewis, 1909.) V.card.ant., vena cardinalis anterior; V., v. cardinalis communis; V .card. -post., v. cardinalis posterior; V.ling.fac, v. linguo-facialis; V.scl.d., v. subclavia dorsalis; Vscl.v., v. subclavia ventralis;, v. thoraco-epigastrica; V.ul.p., v. ulnaris prima.

chief vein in the adult limb, its distal superficial territory is soon greatly exceeded by the development of the v. cephalica.

In embryos of ten millimetres and under, the proximal portion of the ulnar border vein, after receiving the thoraco-epigastric vein from the lateral body wall, drains into the posterior cardinal or common cardinal vein by taking a course dorsal to the brachial plexus and subclavian artery (Fig. 474, F. T. Lewis). Shortly after this stage, however, a venous path is also found ventral to these structures, and after a short time, during which the brachial nerves are enclosed in a venous ring (Fig. 475), the dorsal path finally For some reason the limb capillaries will not approach very close to the ectodermal covering of the limb bud, but leave a narrow sub-ectodermal zone of mesenchyme non-vascular; hence the marginal vein which is formed from the " frontier line " of these capillaries follows faithfully the boundary of the rim.

84 Hochstetter observed in living embryos that the direction of blood flow for practically the entire extent of the border vein of the upper limb is from before backward, i. e., into the ulnar extremity.

Fig. 476. — Reconstruction of the veins of the right arm in a human embryo 16 mm. long. (After F./T. Lewis, 1909.) V. ceph., v. cephalica. For other abbreviations see Figs. 85 and 86.

Fig. 477. — Reconstruction of the right shoulder region in a human embryo 22.8 mm. long. (After F. T. Lewis.) Ribs, clavicle, scapula, and humerus have been stippled and the subclavius muscle has been drawn. V. an.dext., v. anonyma dextra; V. an. sin., v. anonyma sinistra; V. br., v. brachialis; V. ceph., v. cephalica; V. jug. ant., V.jug.ext., V. jug. int., v. jugularis anterior, externa, et interna; v. mammaria interna.

atrophies. Moreover, while the subclavian vein at first opens into the posterior 'cardinal, it eventually is found joining the duct of Cuvier, and in still older embryos (16 mm.) the anterior cardinal or jugular rein, a phenomenon to he associated with the descent of the heart and main vessels into the thorax.

The cephalic vein is entirely secondary, and appears first in man, as in the rabbit (Fig. 469), ° 5 as a small vessel which collects the blood from the outer side of the hand plate and fore-arm anlage and flows into the radial end of the ulnar border vein near the elbow. 96 Very soon this vein can be traced upward along the

Fig. 478. — Reconstruction of the relations of the great veins of the arms and neck in a human embryo 20 mm. long. (Mall collection, No. 349.) radial side of the upper arm (Figs. 476, 477), and in an embryo of 22.8 mm. Lewis has shown that the cephalic vein now joins the external jugular, an arrangement which is true for the embryo figured in Fig. 478, but in which there is also now present a connection between the cephalic and the subclavian veins which is to function as the definitive proximal ending of the cephalic vein in man. This earlier drainage channel of the cephalic into the external jugular vein may persist (jiigulocephalic rein), as has been noted for many years in descriptive human anatomy.

The cephalic vein at the stage last mentioned has become the chief superficial vein of the arm, for, with the breaking up of the border vein by the outgrowth of the digits and the formation of interdigital veins, we have a transferral of the latter veins to the system of the v. cephaliea, which now, collecting its blood from the back of the hand, courses along the radial border of the forearm and arm entirely distinct from the ulnar border vein (the v. basilica, Fig. 479). As is well known, in the adult these two great veins are connected in a wide-meshed plexus. A complete injection

  • > Compare with Hochstetter's figure 2 a, Taf . III. Morpli. Jahrb., 1891, for the rabbit.

" This connection of basilic and cephalic veins has nothing to do with the v. mediana cubiti, which is a late connection and formed long after the primitive junction of the two vein? has disappeared and they have existed as two independent channels. (See beyond.)

Fig. 479. — and Fig. 480. — The superficial veins of the right arm in a human fetus 35 mm. long. From an injection. (The specimen is the same as that shown in Fig. 473.) of the arm veins in an embryo 35 mm. long shows thai even at this stage there are not yet formed the many connections between basilic and cephalic veins which constitute the well-known venous plexus of the dorsum mani and the forearm. It is thus possible to state that the great subcutaneous venous plexuses of the extremity are not partial remains of a primary embryonic more extensive plexus, for the only primary plexus existing here is again a general capillary mesh, and the larger venous connections which characterize the adult are clearly secondary formations. In the arm figured, one may see the earliest veins of the volar surface of the forearm, and, especially clearly, the method of formation of the v. mediana antibrachii through the enlargement of parts of the general capillary mesh (Fig. 480).

In the posterior limb bud it has already been mentioned that the superficial portion of the fibular border vein persists, for it can be identified in a series of embryos (15.5, 20, 23, and 26 mm. long) and seen to constitute the v. saphena parva. The

Fig. 481. — The fibular border vein in a human embryo 15.5 mm. long. (Mall collection, No. 390.) (After a sketch kindly placed at my disposal by Mr. Max Broedel.)

Fig. 482. — The fibular border vein in an injected human embryo 21 mm. long. (Mall collection, No. 460.) The vein is seen to drain the dorsum of the foot by a distinct venous arch; the proximal portion of the original border vein can be recognized.

deep portion of this vein accompanies the sciatic artery and nerve in the region of the thigh and through the foramen ischiadicum into the pelvis ; it is hence the v. ischiadica. It joins the posterior cardinal vein, of which it constitutes the chief radicle, for the caudal vein (v. sacralis media) is inconspicuous. At a later stage (Fig. 485) the vein formed from the union of the femoral and great saphenous veins joins the proximal portion of the ischiadic vein just before the latter ends in the v. cardinalis posterior. In human embryos measuring 10 mm. or less, the ischiadic vein constitutes the chief drainage channel of the lower limb, but in its superficial extent the vein is soon exceeded by the v. saphena magna, a secondary channel, and in its deep territory by the v. femoralis, which has developed along the permanent artery (a. femoralis) of the limb (the v. ischiadica in the adult being important only as a collateral path for the blood). The early

Fig. 483. — The fibular border vein (v. saphena parva) in a human embryo 23 mm. long (Mall No. 462) at a time when toes and heel are clearly evident.

Fia. 484. — Drainage of the perineum and buttocks into the v. saphena magna, in a human fetus 50 mm long. (Mall No. 458.) (From an injection by Mr. Broedel.) development of the v. saphena magna in man is not known, but at the stage of 23 mm. it already constitutes the chief superficial vein of the leg.

In embryos of 24 and 25 mm. length, anastomoses on the inner side of the thigh have begun to direct the blood stream in the

696 saphena parva to the v. saphena magna, and in an embryo measuring 35 mm. and in three embryos of approximately 50 mm. in

V. cava inf.

V. epigastrica Vena femoralis superficialis superficialis externa

V. saphena magna

V. saphena parva

Vv. saerales media? Fig. 4S5. — Reconstruction of the chief veins of the pelvis and lower extremities in a human embryo 20 mm lone. (Mall collection, No. 349.)

V. femoralis superficialis externa

V. saphena magna

V. saphena parva (v. saphena accessoria) Fig. 486. — The superficial veins of the leg in a human fetus 35 mm. long. (After an injection of the living embryo; secured through the kindness of Dr, Thos. Cullen.) (Mall, No. 449.)

length, I have found this connection a constant feature, practically all the blood of the lower leg vein {v. saphena parva) going into the greater saphenous channel. 97 In the youngest of these embryos the saphena parva continues up the inner side of the thigh before joining the saphena magna (a condition which lias heen observed as a variation in the anatomy of the adult for a long time), but in all the other cases the small saphenous vein pours its blood into the v. saphena magna near the knee. Eventually the v. saphena parva joins the deep vein {v. femoral is) in this neigh

V. .-aphena accessoria

V. saphena magna

Fig, 487. — The superficial veins of the leg in a human fetus 50 mm. long. (After an injection by Mr. Broedel.) borhood, as is well known to be its definite normal ending, although in a great percentage of cases the connection here with the saphena magna is also retained to form a subsidiary channel {e.g., Quain's Elements of Anatomy, 10th Ed., Vol. II, Part II, p. 538, London 1894.)

"Whether Ave are dealing here with a general fact or not is impossible as yet to decide. If such is not the case, it must be remarked as unusual that I have found the six lower limbs of the three embryos measuring fifty millimetres to be absolutely indentical in this respect. I note also that Bardeleben refers to a .similar arrangement of the saphenous veins. " Ferner mundel bei jenen (d. h. Feten) die v. saphena parva, welche der basilica homolog ist, in die saphena magna" (Bardeleben, 1880, p. 604).

In the development of the leg, the proximal portion of the extremity is for a while buried, as it were, in the tissues of the embryo, and only in embryos of some 20 mm. in length, and in those older than this, can we speak of a cutaneous surface belonging to the inner side of the thigh. Consequently the saphena parva is in the position to drain the early venules which come from the neighborhood of the perineum and buttock (if we may yet speak of the latter), as Fig. 481 will show. With the "pushing out" of the thigh, this is no longer possible,[1] for the proximal end of the saphena parva is carried out with the knee, and the saphena magna is now the direct and natural channel for this blood. In embryos measuring 50 mm. in length the vessels draining the back of the buttocks into the saphena magna constitute a large and prominent system (Fig. 484).

As Bardeleben first indicated and as has been shown by the work of Hochstetter and of Lewis, the limb veins which are true accompanying vessels to the arteries are the last to develop.[2]


  1. Except, of course, in those eases in which, as in Fig. 4S6, the saphena parva continues up the inner side of the thigh.
  2. Mention may here be made of the occurrence of a prominent " superficial external femoral " vein which drains the front and outer side of the thigh and joins the saphena magna near the fossa ovalis (embryos of 23 and 35 mm.). It is relatively large in these embryos, by far the greatest tributary of the saphena magna. The vein is recognized as common in the adult {e.g., Quain, Spalteholz, Piersol, etc.). In the 35 mm. embryo it was remarkable that on both sides the vein began suddenly by deep roots in the region of the knee — the latter streamed from the vascular plexus surrounding the cartilage of the lower end of the femur and turned out sharply to the skin.



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Vebsari, R. : Morfologia dei vasi sanguigni ai-teriosi dell' ochio dell' uomo e di altri mammiferi. Rieerche fatte nel Lab. d. Anat. umana norm, della R. univ. di Roma. Vol. 8. Fase. 3-4. 1900. La morphogenese des vaisseaux sanguines de la retine humaine. Periodico del Lab. d. Anat. norm, della R. univ. di Roma. Vol. 10. Fase. 1. 1903. Ueber die Entwicklung der Blutgefasse des menschlichen Auges. Anat. Anz. Bd. 35, Nr. 4. 1909.

Vriese, B. de : Reeherehes sur revolution des vaisseaux sanguins des membres chez l'homme. Arch. Biol. T. IS, p. 665-730. 1902. Ueber die Entwicklung der Extremitiiten bei den Saugetieren. Verh. d. Anat. Ges. 16. Vers. Halle a. S. Erg.-Heft z. Anat. Anz. Bd. 21. 1902. Sur la signification morphologique des arteres cerebrates. Arch. Biol. T. 21, p. 357-455. 1905. Reeherehes sur la morphologie de l'artere basilaire. Diss.-Inaug. Univ. Gand. 1905.

Young, A. H. : On the Termination of the Mammalian Aorta, with Observations on the Homologies of the Pelvic Arteries. Stud. Anat. Dept. Owens College. Vol. 1, p. 209-225. 1891. Abnormalities of the Middle Sacral Artery and their Morphological Significance. Journ. of Anat and Phys. Vol. 31; and Studies in Anat. from Anat. Dept. Owens College. Vol. 2, p. 41. 1897. Observations on the Lumbar Arteries. Journ. of Anat. and Phys. Vol. 39, p. 295; and Studies in Anat. from Anat. Dept. University of Manchester. Vol. 3. p. 129. 1906.

Young, A. H., and Robinson, A.: The Posterior End of the Aorta. Journ. of Anat. and Phys. Vol. 32. 189S. Observations on the Development and Morphology of the Tail. Brit. Med. Joum. Vol. 2, p. 1384-1391. 1904.

Young, A. H., and Thompson, P.: Abnormalities of the Renal Arteries, with Remarks on their Development and Morphology. Joum. of Anat. and Phys. Vol. 38. 1903. Zagorsky: Mem. de l'acad. des Seienc. de St. Petersbourg. Vol. 1, p. 326. 1809.

Zimmekmaxx, W. : Ueber die Kiemenarterienbogen des Menschen. Verb. d. 10. internat. med. Kongr. Berlin. Bd. 2. Abt. 1. 1S90. Ueber emen zwischen Aorten und Pnlmonalbogen gelegenea Kiemenarterienbogen beim Kaninchen. Anat. Anz. Bd. 4, S. 720. 18S9.

Zuckerkaxdl : Ueber die Entstehung der Vorderarnigefasse beim Kaninchen und bei der Katze. Verb. Anat. Ges. Erg.-Heft z. Anat. Anz. Bd. 8, S. 126-129. 1893. Zur Anatomie und Entwieklungsgesehichte der Arterien des Vorderarmes. Anat. Hefte. Bd. 4, S. 1-98. 1894. Ebenda. Bd. 5. 1895. Zur Anatomie und Entwieklungsgesehichte der Arterien des Untersehenkels. Anat. Hefte. Bd. 5. 1895.

Histogenesis of the Arterial Wall

Argaud, R.: Recherches sur la structure des arteres chez l'homme. 4 Taf. Toulouse 1903. Sur la .structure du canal arteriel chez le foetus du oeme mois. Toulouse 1905.

Aschoff, A. : Beitrag zur Entwieklungsgesehichte der Arterien beim menschlichen Embryo. Schwalbe's Morph. Arb. Bd. 2. Heft 1. S. 1-35, auch Diss. Strassburg 1892. Ueber Entwicklungs-, Waehstums- u. Alters- Vorgiinge a. d. Gefassen vom elast. u. musk. Typus. Jena 1909.

Grunstein, N. : Ueber den Bau der grosseren menschlichen Arterien in verschiedenen Altersstufen. Arch. f. mikr. Anat. Bd. 47. 1896. Ueber den Bau der Wandung der Blutgefasse. Sitz.-Ber. d. Niederrh. Ges. f. Naturw. u. Heilk. in Bonn. 10. Febr. 1S96.

Morpurgo, B. : Ueber die Entwicklung der Arterienwand. Sitz.-Ber. d. kais. Akad. d. Wiss. Wien 1885.

Priebatsch, K. : Ueber die Histogenese der Aortenwand der Saugetiere mit be sonderer Beriieksichtigung der elastischen Fasern. Diss. Bern 1903.

Roeder, H. : Die Histogenese des arteriellen Ganges, ein Beitrag zur Entwicklungs meehanik der Petalwege. Arch. f. Kinderheilk. Bd. 33, S. 149-161. 1902.


Anikiew. A.: Zur Frage iiber die Entwicklung der vena anonyma sinistra. Anat. Anz. Bd. 34, S. 24. 1909.

Bardeleben, K. vox: Die Hauptvene des Ai'mes, vena capitalis braehii. (Ueber die Entwicklung der Extremitatenvenen des Menschen.) Jenaische Zeitschr. f. Naturw. Bd. 14. 1879.

Benigxi, E. : Persistenza della vena ombilicale nelF adulto. Gazz. Ospidali. Anno 25. N. 85, p. 894-895. Bonnot and Seevers: On the Structure of a Human Embryo Eleven Millimetres in Length. Anat. Anz. Bd. 29, S. 452-459. 1906.

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Davis. D. M. : Studies on the Chief Veins in Early Pig Embryos and the Origin of the Vena Cava Inferior. Amer. Joum. of Anat. Vol. 10, p. 161-472. 1910.

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Hoffmann, C. K. : Zur Entwicklungsgeschichte des Yenensystems bei den Selaehiern. Morph. Jahrb. Bd. 20. 1893. Kolliker, A. : Entwicklungsgeschichte des Mensehen und der hoheren Tiere. Leipzig 1879.

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العربية | català | 中文 | 中國傳統的 | français | Deutsche | עִברִית | हिंदी | bahasa Indonesia | italiano | 日本語 | 한국어 | မြန်မာ | Pilipino | Polskie | português | ਪੰਜਾਬੀ ਦੇ | Română | русский | Español | Swahili | Svensk | ไทย | Türkçe | اردو | ייִדיש | Tiếng Việt    These external translations are automated and may not be accurate. (More? About Translations)

Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia.

XVIII. Development of Blood, Vascular System and Spleen: Introduction | Origin of the Angioblast and Development of the Blood | Development of the Heart | The Development of the Vascular System | General | Special Development of the Blood-vessels | Origin of the Blood-vascular System | Blood-vascular System in Series of Human Embryos | Arteries | Veins | Development of the Lymphatic System | Development of the Spleen
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العربية | català | 中文 | 中國傳統的 | français | Deutsche | עִברִית | हिंदी | bahasa Indonesia | italiano | 日本語 | 한국어 | မြန်မာ | Pilipino | Polskie | português | ਪੰਜਾਬੀ ਦੇ | Română | русский | Español | Swahili | Svensk | ไทย | Türkçe | اردو | ייִדיש | Tiếng Việt    These external translations are automated and may not be accurate. (More? About Translations)

Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia.

Manual of Human Embryology II: Nervous System | Chromaffin Organs and Suprarenal Bodies | Sense-Organs | Digestive Tract and Respiration | Vascular System | Urinogenital Organs | Figures 2 | Manual of Human Embryology 1 | Figures 1 | Manual of Human Embryology 2 | Figures 2 | Franz Keibel | Franklin Mall | Embryology History