Paper - The development of the veins in the limbs of rabbit embryos

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Lewis FT. The development of the veins in the limbs of rabbit embryos. (1905) Amer. J Anat. 5: 113-120.

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This historic 1905 paper by Frederic Thomas Lewis (1875—1951) describes development of the veins in the limbs of rabbit embryos.

This paper uses models based on the Harvard Embryological Collection.

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

Modern Notes: rabbit | limb | vein

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The Development of the Veins in the limbs of Rabbit Embryos

Frederick Thomas Lewis
Frederick Thomas Lewis (1875-1951)


Frederic T. Lewis.

From the Embryological Laboratory, Harvard Medical School.

With 1 text figure.


In connection with the preceding study of the lymphatic system it was necessary to reconstruct the veins of the shoulder and hip in a series of rabbit embryos. The reconstructions were then extended to include the distal portions of these vessels, complete figures of which had never been published. Hochstetter, in 1891, had observed the veins in the limbs of living rabbit embryos, and had studied them in serial sections. His drawings, however, show only detached portions of the veins such as could be seen under most favorable conditions, in living embryos. Ten years later Grosser described but did not reconstruct, the developing veins in the extremities of bats. To these two investigators embryology is indebted for the present knowledge of the veins in mammalian limbs. It is proposed to review their work, while describing the reconstructions, considering first the veins of the anterior extremity, then those of the posterior extremity, and finally the homologies which exist between the two sets.

Veins of the Anterior Extremity

In the youngest rabbit figured, an embryo of 13 days, Fig. 1, p. 97, the small vessels along the radial or anterior border of the arm unite to form a vein which follows the periphery of the limb to its posterior or ulnar border, and then ascends behind the brachial plexus to terminate near the junction of the anterior and posterior cardinal veins. It receives a branch which at this stage is not well defined, ascending in the body wall. This is the Seitemumpfocae of Hochstetter, and becomes the external mammary vein of the adult.

According to Hochstetter, in rabbits of 12 and 121/2 days, the “ border vein” makes a complete circuit of the limb, and its radial part either empties into the ulnar vein near its termination or connects with the cardinal vein directly. But this radial vein is said to be hard to follow because “ attended by several venous twigs of nearly the same caliber, and only shortly before its termination is it recognizable as a d.istinet (starkeres) vessel ” (p. 24). In a 13-day rabbit the radial vein had disappeared, “since it had been but imperfectly marked out.” Similarly Grosser found a radial vein emptying into the anterior cardinal close to the ulnar vein, in the youngest bat which he studied (4% mm.). In the next stage (614 mm.) it had vanished (p. 136). An examination of rabbits of 12 and 121/2 days, together with younger ones in the Harvard Collection,-shows that the first vein of the arm develops along its ulnar margin, extending distally around the border to the radial side. Small and variable vessels such as Hochstetter described as a radial vein may occur, as shown in Fig. 1, p. 97, but they do not form a structure comparable with the primitive ulnar vein. The latter may be called the primary vein of the -arm.

The rabbit of 14 days, Fig. 2, p. 98, presents the condition described by Hochstetter in embryos of 13 days. The primitive ulnar vein has acquired a new outlet ventral to the brachial plexus, so that, by the persistence of the original dorsal termination, most of the plexus and the brachial artery are surrounded by a loop of vein. In the following rabbit, Fig. 3, p. 100, the ventral outlet of the ulnar vein is the chief one. This specimen shows a small vessel extending from the external jugular vein toward the radial border of the arm.

The next embryo, Fig. 4, p. 102, is considerably more advanced. The dorsum of the hand, which was previously its external surface has rotated and become anterior; the arm is in pronation. The difierentiation of the

fingers is indicated by the sinuous terminal border of the hand, and by shallow interdigital depressions on its dorsum. Beneath these, interdigital veins have been formed, probably from branches of the primitive ulnar vein. A new vein has grown from the external jugular down the anterior or radial border of the arm, and has united with the independently formed interdigital veins. This is the cephalic vein of the adult. It is embryologically the second vein of the arm.

Hochstetter states that the cephalic vein in rabbits develops toward the body from the back of the hand, connecting with the ulnar vein at the elbow, and later continuing up the arm to the external jugular vein. The preceding reconstructions, of the rabbit agree better with Grosser’s description of the bats. He failed to find a stage in which the cephalic vein emptied into the ulnar. In the earliest specimen in which the cephalic vein was found, it connected with the external jugular vein.

The cephalic vein of the 17-day rabbit is the chief vein of the limb, and has developed a branch which follows the radial artery, the deep radial vein, Fig. 7, p. 107. At 20 days, Fig. 8, p. 108, the cephalic vein has acquired its new and permanent orifice near the axillary vein. The jugulo-cephalic vein marks its former outlet.

With the differentiation of the digits, the primitive ulnar vein becomes greatly reduced by the loss of its distal portion. This is shown in Fig. 4. At 17 days, Fig. 7, p. 107, the continuity of the primitive ulnar vein has been interrupted at the elbow, resulting in further reduction. The vein then extends from the elbow to the superior vena cava, following the brachial artery, from around which it receives small branches. In the 20-day embryo, Fig. 8, p. 108, the brachial vein (proximal part of the primitive ulnar) is continued down the forearm following the ulnar artery. If we may judge from the position of this vessel, there has been a re-establishment of the course which was interrupted in the younger embryo. I-Ioch-stetter, however, states (p. 28) that in rabbits the forearm section of the primitive ulnar vein seems to dis-appear, although in m-an (p. 33) the corresponding vessel is preserved throughout, and forms the basilic vein of the forearm and arm, the axillary and subclavian veins.

The question arises whether the primitive ulnar vein should be described as producing the deep ulnar, brachial, and axillary veins, naming it for the adjacent arteries, or as forming the basilic and axillary veins, considering the cutaneous vein of the corresponding region as its more direct derivative. This uncertainty calls attention to the fact that both the superficial and deep sets of veins have a common origin, and that before their separation the embryonic vein may properly be _called either brachial or basilic. The rabbit of 20 days is characterized by the establishment of this brachial (or basilic) vein.

In the development of the veins of the arm three stages have been distinguished:

  1. The stage of the primitive ulnar vein.
  2. The stage of the primitive cephalic vein.
  3. The stage of the primitive brachial vein, the cephalic vein persisting.

Veins of the Posterior Extremity

A rabbit of 10.5 days (Harvard Collection, No. 199) has a very large umbilical vein which sends branches into both limbs. Those in the leg form a net which connects with the posterior cardinal vein, still a minute vessel in the caudal end of the body. From the network a vein is developed, which after following the periphery of the limb and passing along its posterior or fibular border, empties into the cardinal vein. This vessel may be called the primitive fibular vein. The original connections of the 116 Development of the Veins in the Limbs of Rabbit Embryos

net with the umbilical vein do not form a well defined vessel and soon disappear. Although Hochstetter recognizes this, he refers to the connection with the umbilical vein as a tibial border vein. Grosser could not identify such a vessel in any of his three youngest bats (p. 149).

The primitive fibular vein as shown in Fig. 2, p. 98, is a vessel readily comparable with the primitive ulnar vein. Both course along the posterior borders of their respective limbs, in which they are the first veins developed. They are undoubtedly homologous. In later development, however, they constantly diverge from one another. Even at 14 days the fibular vein has two small branches which are not matched by any belonging to the ulnar vein. One of these. coming from twigs on the outer and caudal surface of the leg, becomes the anterior tibial vein, An. T. The other which extends mediad toward what at this stage is the inguinal line, may be referred to as the “ connecting branch,” 0. b. In the more advanced embryo, Fig. 3, p. 100, the same branches appear in similar relations. They have become much larger at 14 days 18 hours, Fig. 4, p. 102. Here the anterior tibial branch has extended diagonally down the limb to the dorsum of the foot. The connecting branch has sent its twigs into the abdominal wall and the adjoining tibial border of the limb. The primitive fibular vein is still the chief vein of the leg.

In the older rabbit, Fig. 7, p. 107, the differentiation of the toes has broken up the distal portion of the primitive fibular vein, which has‘disappeared almost to the point where it receives its anterior tibial branch. This branch now arises from the interdigital veins on the dorsum of the foot and its main trunk appears continuous with the proximal part of the primitive fibular vein. The anterior tibial and primitive fibular veins together, now constitute the sciatic vein, which is embryologically the second vein of the leg.

The reconstructions to which we have referred agree with Hochstetter’s description of the development of the sciatic vein except in one detail. They do not show that a part of the primitive fibular vein distal to the anterior tibial branch persists as the small saphenous vein.

"In the rabbit of 14 days 18 hours, a third vein of the leg has begun its development. This is the femoral vein which terminates in the posterior cardinal anterior to the sciatic vein. It advances toward the tibial border of the limb. At 17 days, Fig. 7, p. 107, it is seen approaching the external mammary and the connecting branch of the sciatic vein. In the embryo of 20 days, Fig. 8, p. 108, it has anastomosed with both and passes down the leg as the posterior tibial vein, Po. T.

Just as it is questionable in the arm whether the parent vessel should be designated brachial or basilic, so in the leg there is the choice between femoral and large saphenous vein. Both of the latter spring from the vessel which we have called femoral. The close relation between the two is shown by Krause’s description of the veins in the adult rabbit, where the posterior tibial is considered to be the distal continuation of the large saphenous vein. It seems probable also, that the anteror tibial vein, which is quite superficial at 20 days, though it accompanies the artery, should give rise to the small saphenous vein, with which it anastomoses in the adult. Hochstetter, as already noted, assigns a somewhat different origin to the small saphenous vein.

The condition found in the rabbit at 20 days, is essentially that of the adult. The sciatic vein remains a large vessel. In man, assuming that the embryological history is similar to that of the rabbit, the proximal section of the sciatic vein dwindles after the formation of the femoral anastomosis near the knee. The sciatic vein is represented, therefore, merely by the collateral circulation of the thigh, as figured by Charpy (Poirier’s Anatomic, Vol. 2, p. 1052), and by Spalteholz (Handatlas, Vol. 2, p. 469).

The preceding observations seem to establish three stages in the venous development of the leg, comparable with those in the arm.

  1. The stage of the primitive fibular vein.
  2. The stage of the primitive sciatic vein.
  3. The stage of the primitive femoral vein, the sciatic vein persisting (in man, very much reduced).

Homologies Between the Veins of the Anterior and Posterior Extremities

Bardeleben’s view that the primary veinof the arm consisted of the vena cephalica autibrachii, vena median-a cubiti, and vena basilica brachii, and that this was homologous with the vena saphena magna of the leg was rightfully criticized and condemned .by Hochstetter. Nevertheless it is referred to somewhat favorably by Charpy.

Krause finds that the cephalic and sciatic veins are analogous (p. 210). Hochstetter denies this, and arrives at the following concluions. Since the ulnar and fibular borders of the limbs are homologous, the primitive veins which follow them are also homologous. The small saphenous vein and the basilic vein of the forearm, being presumably persistent portions of the primitive veins, are therefore homologous. The cephalic and large saphenous veins are secondary formations, and any comparison between 118 Development of the Veins in the Limbs of Rabbit Embryos

them is uncertain. The femoral and braehial veins “ show no agreement either in position or in origin ” (p. 35).

These conclusions clearly depend upon the serial homology of the limbs. If We should accept the idea of inverse homology, advocated by Wilder, Wyman, and others, according to whom the thumb is comparable with the little toe, and the radial border with the ulnar, then conclusions almost the reverse of Hochstetter’s would be expected. A third basis for comparison is supplied by the familiar rotation theory. According to it, the limbs are at first serially homologous. The thumb and great toe, the ulnar and fibular borders correspond. The external surfaces of both limbs are to be extensor and the inner surfaces flexor. Later a rotation of approximately 90° occurs in both limbs, but in opposite directions. The extensor surface of the arm becomes posterior, and that of the leg becomes anterior. The knee and elbow are thus brought to bend in opposite directions. The foot is rotated with the leg and its extensor surface (dorsum) is directed anteriorly. The hand is not rotated with the arm, but ordinarily in the reverse direction, so that its extensor surface is directed anteriorly like that of the foot. Since the arm and hand are rotated in opposite directions, a crossing of the bones of the forearm is produced. In man the hand may, in later development, be rotated with the arm so that its dorsum looks posteriorly and the bones of the forearm are not crossed. In this position the inverse symmetry of the arm and leg is complete.


DIAGRAM. 1. Anterior view of the arm and leg in their three stages of venous development. In Stage 1, a and _A show the arm and leg, respectively, before rotation; b and B, after rotation. The primitive ulnar and flbular veins are in solid black. The secondary cephalic and sciatic veins are drawn as double lines, and the tertiary brachial and femoral veins have transverse shading. The black lines in contact with the secondary and tertiary vessels indicate the portions of those veins which are formed from the primitive vessels of Stage 1.

The embryonic rotation of the limbs is not to be compared with their voluntary rotation in the adult, for the former is a complex shifting of tissues involving modificati-ons in the shapes,of the bones. These changes in the human leg -are clearly shown by Bardeen’s reconstructions in Vol. 4 of this journal. (Compare Figs. 3, 5, 9, 12-, and 13, following p. 302.) The external appearances during rotation may be observed in the rabbit embryos figured by Minot and Taylor for Keibel’s Normentafeln. From these it will be seen that rotation does not occur with mathematical precision.

Interpreted according to the rotation theory, the fundamental veins of the arm correspond with those of the leg. Their homologies are shown in the accompanying diagram which is based upon the reconstructions previously described. The diagram presents throughout anterior views of the left limbs, the veins being drawn as they would appear if the limbs were transparent. In Stage 1, at a. and A respectively, the arm and leg are shown before rotation. Serial homology between the primitive ulnar and fibular veins is complete. Then rotation occurs, whereby the fibular vein is carried from the posterior to the outer border of the leg, as shown at B. The arm, on the contrary, turns so that the ulnar vein is carried from the posterior to the inner border, as in b. ‘The forearm rotates in the opposite direction from the upper arm, so that the ulnar vein crosses from the inner side above to the outer side below. Were the forearm in supination, the ulnar border would be internal throughout. After rotation the ulnar border is no longer homologous with the fibular, but corresponds with the tibial border.

In Stage 2, veins are established along the inversely homologous external borders of the limbs, the radial and fibular respectively. As shown in the diagram, the cephalic vein must be a new formation throughout, but the course of the sciatic vein is already partially occupied by the primitive fibular vein. Consequently the sciatic may incorporate a portion of the fibular vei.n. Thus it appears that a real homology exists between the cephalic and sciatic veins, although, as Hochstetter pointed out, they differ in their relations to the primitive veins of the limbs.

In Stage 3, the brachial and femoral veins develop along the inversely homologous ulnar and tibial borders. In this case the vein of the arm may incorporate the remains of the primitive ulnar vein, as was found to occur in rabbit embryos. The femoral vein on the contrary must be new throughout.

Thus the primitive ulnar and fibular veins, which develop before rotation, are serially homologous. The veins arising after rotation may be considered inversely homologous, the cephalic with the sciatic, and the brachial with the femoral.

Literature Cited

BABDEEN, CHARLES R., 05.— Studies of the Development of the Human Skeleton. Amer. Journ. of Anat., Vol. 4, pp. 265-302.

CHARPY, A., 95 —Tra.ite d’Anatomie Humaine. Edited by Paul Poirier. Vol. 2. Paris.

Gnossnn, Orro, o:.—Zur Anatomie und Entwickelungsgeschichte des Gef§.sssystemes der Chiropteren. Anat. Hefte, Abt. 1, Vol. 17, pp. 203-424.

HOCHSTETTER, FERDINAND, 91.—Ueber die Entwicklung der Extremitiitsvenen bei den Amnioten. Morph. Ja.hrb., Vol. 17, pp. 1-43.

KRAUSE, W., 6s.—Die Anatomie des Kaninchens. Leipzig.

Minot CS. and Taylor E. Normal Plates of the Development of the Rabbit Embryo (Lepus cuniculus). Vol. 5 in series by Keibel F. Normal plates of the development of vertebrates (Normentafeln zur Entwicklungsgeschichte der Wirbelthiere) Fisher, Jena., Germany.

SPALTEHOLZ, WERNER, o:.—Ha.ndatlas der Anatomie des Menschen. Vol. 2. Leipzig.

WILDER, Bonn: G., 7:.—Intermembral homologies. Proc. of the Boston Soc. of Nat. H1st., Vol. 14, pp. 154-242.

WYMAN, JEFFRIES, 57.—0n symmetry and homology in limbs. Proc. of the Boston Soc. of Nat. Hist., Vol. 11, pp. 246-278.

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