Paper - The development of the arteries of the human lower extremity

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Senior HD. The development of the arteries of the human lower extremity. (1919) Amer. J Anat. 22:1-11.

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This historic 1919 paper by Senior described development of the arteries in the lower limbs. Note the later correction published in 1920 paper. Senior HD. The development of the human femoral artery, a correction. (1920) Amer. J Anat..


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The Development of the Arteries of the Human Lower Extremity

H. D. Senior

Department of Anatomy, New York University

Eleven Figures

I. Introduction

a. General Considerations

It is well known that considerable differences exist between the various types of arterial distribution which are nor encountered in the pelvic limb of the different representatives of the mammalian series. In all mammals in which the developmental history of the arteries of the limb has been investigated, however, it has been found that the adult arterial system of the part results from the elaboration of two embryonic vessels. Both of the embryonic arteries in question take origin from the dorsal (secondaiy) root of the a, umbilicalis. One of them, the primitive artery of the limb, traverses the axis of the thigh and leg and divides into a number of branches for the supply of the foot. This vessel is present before the limb forms a distinct prominence upon the surface of the body and is known as the axial or ischiadic artery.


The other is an artery of later development which traverse the pelvis and the ventral region of the thigh. It joins the axial artery a short distance above the knee and gives rise to the a. iliaca externa, the a. femoralis, and the a. epigastrica inferior and to the branches which arise from these vessels. All other arteries of the limb arise from the axial artery itself or from the branches to which it gives origin.


Whether the relations of the embryonic axial artery to the other constituents of the limb are identical in the embryos of all mammalian forms is a question to Avhich direct observation of the vessel has not yet furnished an answer. Much indirect evidence bearing upon this subject is furnished by Zuckerkandl's comparative study of the arteries of the leg which appeared in 1895.


The study in question, although it is mainly concerned with the relations of the adult arteries, is influenced throughout by embryological considerations. It includes, in fact, a study of the arteries in a series of vertebrate embryos in which the mammalia are represented by the rabbit and cat. Zuckerkandl's work is obviously based upon the conception of the identity of the course of the axial artery throughout the mammalian series. It may be said that the general results of the investigation are greatly in favor of the correctness of the author's conception.


The principal relations of the axial artery of the embryo have been established by the present study. An adequate account of the relations of this and other arteries of the developing limb of one of the quadruped mammals would be of great value for purposes of comparison.

only consecutive account which has been given of the development of the arteries of the pelvic limb in any mammalian form is that of DeVriese, which appeared in 1902. It deals with the human embryo. The other papers contained in the literature of the subject are concerned with isolated stages in the development of one or more forms rather than with a complete history of the arteries of any particular mammal.


Hochstetter showed for the first time, in 1890, that the primitive artery of the mammalian thigh, which he termed the a. ischiadica, follows the course of the n. ischiadicus in the embryos of both the cat and the rabbit. He also described the development of the a. femoralis, which, appearing at a later stage, supersedes the proximal part of the a. ischiadica as the artery of the thigh. The secondary assumption of the original function of the a. ischiadica by the a. femoralis was shown to occur in man by DeVriese in 1902.


Hochstetter did not succeed in following the continuation of the a, ischiadiea through the leg. Leboucq, however, described it in 1893, as pursuing, in the human embryo, an axial course between the tibia and fibula and finally perforating the tarsus to reach the dorsum of the foot.

In 1894, Zuckerkandl described the continuation of the a. ischiadiea of the rabbit as traversing the flexor region of the leg and dividhig into a number of branches for the supply of the sole. He also described two branches of the artery which supply the extensor aspects of the leg and foot, respectively. In 1895 the same author described the perforating artery of the tarsus in rabbit embryos and made considerable progress in the nomenclature to the primitive artery of the limb.


In Zuckerkandrs second paper a distinction was made between the terms axial and ischiadic which formerlv had been used more or less interchangeably to denote the primitive artery of the

For the entire artery Zuckerkandl employed the name He restricted the use of the term ischiadic to the part of it which traverses the thiah and used the term a. interossea for the remainder of the vessel. The same paper contained the first accurate description which had been given of the distal part of the axial artery of any mammal. The a. interossea was described in the rabbit as lying between the interosseous membrane and m. tibialis posterior.


Grosser, in 1901, and DcYriese, in 1902, described the a. interossea (the a. nervi interossei cruris of the latter in bat and human embryos, respectively, as pursuing the course it had been described b}^ Zuckerkandl as following in the rabbit.


Both of these observers also recorded the presence, in subjects of their respective studies, of the r. perforans tarsi.

During the course of the present investigation it has become apparent that the existing literature contains no definite statement regarding the course taken by the part of the axial artery which traverses the popliteal fossa. It is questionable whether the popliteal section of the axial artery has been tacitly included as a part of the a. ischiadiea or not, since the distal limit of the latter artery does not appear to have been definitely fixed. In the following description the term a. ischiadica has been restricted to the part of the axial artery proximal to the site at which it is subsequently joined by the a, femoralis. restriction has necessitated the use of a new term for the part of the axial artery which extends from the hiatus tendineus (the approximate site of the femoro-ischiadic junction) to the point (in the neighborhood of the distal border of the m. popliteus) at which the a. mterossea begins.


An examination of the popliteal portion of the human axial artery shows that its distal part does not lie upon the posterior surface of the m. popliteus as does the distal part of the adult a, popliteal but upon the anterior surface of that muscle. It seems clear, therefore, that the distal part of the a. poplitea of the majority of adult mammals, which lies upon the anterior surface of the m. popliteus represents a persisting portion of the embryonic axial artery. On this account the name a. poplitea has been used in the following pages to designate entire popliteal section of the human axial artery.


The solution of Zuckerkandl's difficulty regarding the difference of the mutual relations between the a. poplitea and the m. popliteus in man on the one hand and in the majority of other mammals upon the other has thus been furnished by determining the course of the popliteal portion of the axial artery of the human embryo.[1]


The part of the adult human a. poplitea which extends from the hiatus tendineus to the origin of the a. genu inferior medialis is a direct survival of the embryonic a. poplitea profunda. The part of that artery which lies upon the posterior surface of the m. popliteus is derived from an embryonic vessel of later formation referred to in the following pages as the a. poplitea superficialis.


The literature dealine; with the arteries of the mammalian pelvic limb shows a tendency towards the perpetuation of a conception regarding the relation of the adult human a. peronaea to the embryonic a. interossea which Zuckerkandl has already shown to be erroneous. Stieda stated, in 1893, that the study of the variations of the arteries of the human leg had led him to the conclusion that the a. peronaea represents a persisting portion of the embryonic axial artery. A similar opinion regarding the between these two arteries was expressed by Zuckerkandl in 1894. In 1895 the recognition of the course of the a. interossea led Zuckerkandl to a modification of the views he had previously expressed upon the subject. He drew attention to the fact that it would be impossible for the part of the a. peronaea which is separated from the interosseous membrane by the m. tibialis posterior to be a derivative of the part of the a. interossea which lies between the membrane and the muscle. In 1902 DeVriese revived the conception of the identity of the aa. interossea and peronaea, notwithstanding the obvious justice of ZuckerkandUs contention.


A careful examination of the embryos which form the basis of the present study and of a large number of others belonging to the collection of the Carnegie Institution has been made in the search for a r. saphenus of the a. femoralis comparable in extent to that of the a. saphena which occurs very rarely in adult man and invariably in most of the other mammals. The result has been entirely negative.


That the a. saphena occurs occasionally in the huinan embryo is indicated by the fact that its presence has been noted at least five times in the adult. In the embryos examined in connection with the present study, however, the r. saphenus has not been found to extend in a single instance beyond the middle of the leg.

I take this opportunity of expressing my gratitude to Professor Thyng for the trouble he has taken in the revision of manuscript.

b. Material

In the present investigation the lower extremities of embryos have been studied in seven stages of develop)iient, one extremity or both having been reconstructed in wax. The selection of stages depended upon the accessibihty of well-preserved material rather than upon a preconceived plan regarding the most instructive stages to use.[1]

The following embryos have been studied, the right having been reconstructed in all cases. The embryos of which both lower limbs have been reconstructed are marked with an "+"


Embryo CRL Collection Catalogue No.
6.0 mm+ Carnegie Institution, Embryological Collection (C.T.E.C.) No. 1075
8.5 mm+ Cornell University, Embryological Collection (C.E.C.) No. 9.
12.0 mm+ Cornell University, Embryological Collection (C.E.C.) No. 3.
12.0 mm+ Minnesota, Embryological Collection (M.E.C.) No. H. 16.
14.0 mm Cornell University, Embryological Collection (C.E.C.) No. 5.
17. 5 (?) Harvard University, Embryological Collection (H.E.C.) No. 839.
18.0 mm Carnegie Institution, Embryological Collection (C.I.E.C.) No. 409
22.0 mm Cornell University, Embryological Collection (C.E.C.) No. 1.
Note: The following embryos have been studied, the right having been reconstructed in all cases. The embryos of which both lower limbs have been reconstructed are marked with an "+"
Carnegie Embryos - Senior (1919) - Lower Limb Blood Vessels 
Embryo CRL Collection Catalogue No.
6.0 mm+ Carnegie Institution, Embryological Collection (C.T.E.C.) 1075
8.5 mm+ Cornell University, Embryological Collection (C.E.C.) 9
12.0 mm+ Cornell University, Embryological Collection (C.E.C.) No. 3.
12.0 mm+ Minnesota, Embryological Collection (M.E.C.) H. 16
14.0 mm Cornell University, Embryological Collection (C.E.C.) 5
17. 5 (?) Harvard University, Embryological Collection (H.E.C.) 839
18.0 mm Carnegie Institution, Embryological Collection (C.I.E.C.) 409
22.0 mm Cornell University, Embryological Collection (C.E.C.) 1
Note: The following embryos have been studied, the right having been reconstructed in all cases. The embryos of which both lower limbs have been reconstructed are marked with an "+"
Reference: Senior HD. The development of the arteries of the human lower extremity. (1919) Amer. J Anat. 22:1-11.

For their generosity in placing their material at my disposal, I wish to express my great obligation to Profs. C. M. Jackson, F. T. Lewis, F. P. Mall, C, R. Stockard, and G. L, Streeter.


Toward the end of the investigation, there were a number of difficulties, for the solution of which the examination of rather close intermediate stages was required. Such stages were found in the collection of the Carnegie Institution at Baltimore.


In the formation of this valuable collection, so ably cared for and sympathetically administered. Professor Mall has available to his fellow workers a wealth of material adequate for the solution of any ordinary problem in human embryology.


The reconstruction of vascular plexuses in wax, using every second or fourth section as the case may be, is somewhat difficult. The practice followed has been to unite the parts of the adjacent plates which fit after careful adjustment and to remove those which do not join. In this way the plexus represented in the reconstruction is probably less dense than that occurring in the embryo. The reconstruction in fact, reproduces the spirit rather than the letter of the original.


In reconstructing the stage of 6 mm. consecutive sections were used, and these were comparatively thick (20 um). In this case the parts usually fitted so accurately that the plexuses, as reproduced, must represent, as nearly as possible, the actual conditions in the original.

c. Nomenclature

As already noted, the term a. poplitea profunda is used in the following account to denote the popliteal section of the embryonic axial artery. The term a, ischiadica and a. interossea have been retained for the proximal distal parts of that artery, respectively.

To the artery which normally perforates the tarsus of adult ungulates, and which has been recognized in all embryos hitherto observed, numerous terms have been applied.[2]

The name ramus perforans tarsi is used here.

For two of the embryonic arteries the names used by Hyrtl in 1864 have been retained. They are the r. coronarius (of the medial malleolus) and the a. peronaea posterior superficialis.

The description of a number of embryonic vessels, the existence of which has not been noted heretofore, has necessitated the use of several new terms. These conform, as nearly as may be, with current usage.


In referring to the relative positions of the structures of the limb, the adult terms of orientation have been used throughout. This course has been adopted in order to avoid the confusion which might arise from the alternative use of two sets of terms in making comparisons between the relative positions of structures in the adult and embryonic limb, respectively.


The limb preserves its primitive position which, with the exception of progressively increasing flexion of the knee, remains unchanged throughout the period of development under consideration. The flexor aspect of the embryonic thigh and leg and the plantar aspect of the sole are directed medially; the great toe is preaxial or cephalic. The term posterior for the adult has, therefore, the same significance as the term medial for the embryo; so have, respectively, the terms anterior and lateral, medial and pre-axial, lateral, and post-axial. For the parts above the hip-joint there can be no possibility of confusion, since like terms of orientation serve equally well for the postnatal and embryonic periods.

II. The Arterial System Of The Lower Limb In Progressive Stages Of Development

a. Stage of 6 mm

C. I. E. C, no. 1075, figs, 1 and 9 A

In the lumbar region the nerve roots are not recognizable. The ganglia of the lumbar and sacral regions appear as segmentally disposed swellings upon the continuous neural crest. Distal to the second lumbar segment the postcardinal vein becomes plexiform. The medial part of the plexus receives the segmental veins, the lateral part represents the still indefinite marginal vein.


The dorsal segmental arteries, with the exception of the fifth lumbar and second sacral, pass directly to the spinal cord with arteries, the ventral roots of which are still very large, arise opposite the intervals between the third and fourth lumbar segmentals.


The secondary, or dorsal, roots of the umbiUcal arteries are present, but are smaller than the original or ventral roots of that vessel. Each dorsal root, in the embryo under consideration, arises from the union of two arteries.


The chief share in the formation of the dorsal root of the a. umbilicalis is taken by a vessel which arises from lumbar segmental artery a short distance beyond its root, vessel in question is joined almost perpendicularly near its origin by a smaller one which springs from the aorta in interval between the fourth and fifth lumbar segmental arterie

The dorsal root of the a. umbihcalis; which may be said -to begin at the junction of the two vessels mentioned above, continues the transverse direction of the larger of the two, until it reaches the dorsal aspect of the Wolffian duct of its own side. In this situation it turns vent rally, passing upon the lateral side of the duct, w is now enclosed between the two roots of the umbilical artery, to join the ventral root. As the dorsal root of the a. curves around the lateral side of the Wolffian duct it gives origin to the axial artery of the lower extremity and to the a. pudenda interna.

The axial artery, takes an almost transverse, slightly recurrent, course towards the surface. It ends by dividing into two branches, each of which breaks up into a plexus which passes over into the postcardinal venous plexus. The a. pudenda interna follows the dorsolateral surface of the Wolffian duct towards the urogenital sinus and enters the pelvic arterial plexus.


Senior1919 fig01.jpg

Fig. 1. Reconstruction showing the distal end of the aorta; also the arteries of the right lower extremity and neighboring parts in a human embryo of 6 mm. C.I. E.G., 1075). Medial aspect. X 40 diams.


In addition to the arteries already described, there are two extensive arterial plexuses, which may be called the abdominal pelvic plexuses, respectively. Of these the abdominal arises by seven or eight stems from the concavity of the umbilical artery somewhat distal to the junction of its two roots. It invades the flexor region of the thigh, although it is uncertain to what extent, for the lower limb bud is not distinctly circumscribed at this period.


The abdominal plexus has no connection whatever with the segmental arterial series. It is drained partly by postcardinal plexus, but mainly by the umbiucal vein. The plexus arises by two roots from the convexity of the umbilical artery opposite the roots of the abdominal plexusi It covers the cloaca and receives the pudendal artery and a large branch from the second sacral segmental. It is drained, by the postcardinal plexus. The abdominal and pelvic plexuses appear to be connected by a few vessels passing to the umbilical artery: It is probable that all the visceral branches of the adult a. hypogastrica (excepting the superior vesical) arise out of the primitive pelvic plexus of the original umbilical artery. The branches (as far as they are present before the stage of 22 mm.) arise from, or very near to, the axial artery. They are therefore connected with the dorsal root.[3]

This stage agrees in most essentials with the 5-mm. embryo (II) described by Tandler (^03). The inferior mesenteric artery arises opposite the first lumbar segmental.


b. Stuge of 8.5 mm

C. U. C., no. 9, figs. 2 and 9 B

The femoral, obturator, genitofemoral, and peroneal nerves are readily recognized as short relatively unbranched trunks. The extremity of the tibial is divided into what appear to be the medial and lateral plantar nerves.


The aa. umbilicales have lost their original (ventral) roots now spring from the aorta in the intervals between the fourth and fifth dorsal pairs of lumbar segmental arteries.[4] The fifth lumbar segmental arteries have thus regained their independence, and, like the other segmental arteries in this region, pass to the spinal cord without branching.


The axial artery passes distally into the lower Umb, crossing the n. tibialis posteriorly from the medial to the lateral side. It then follows the posterior aspect of the skeletal mesenchyme throughout the leg into the sole. In the latter situation it breaks up into a flattened plexus which extends somewhat beyond the extremities of the plantar nerves. Just as it is breaking up axial which pierce

Senior1919 fig02.jpg

Fig. 2. Reconstruction showing the arteries of the right lower extremity in a human embryo of 8.5 mm. (C.E.C.; 9). Medial aspect. X 20 diams.

Senior1919 fig03.jpg

Fig. 3. Reconstruction showing the arteries of the right side of the pelvis, right thigh, leg, and dorsum of the foot in a human embryo of 12 mm. (M.E. C.,H. 14). Medial aspect. X 20 diams,

mesenchymal foot reach

Up


perforating branches prod

another flattened plexus- The two plexuses (or retia) of the foot are separated from one another by the mesenchymal skeleton of the foot, the plantar rete lying between the latter and the plantar nerves.


In passing from the medial to the lateral side of the sacro- axial artery runs between the main plexus

The branch referred to has

pudendal plexus, the and a branch from i been removed from the reconstructions illustrated in figures 1 to 6, since it partially covers the artery when viewed from the medial side.


aspect of the concavity of the umbilical artery, some distance proximal to the origin of the axial artery, there now arises a new vessel, the a. iliaca externa. This vessel takes a cephalic direction, nearly parallel to the aorta, coursing medially to the origin of the obturator nerve. At this stage the wall of the external iliac artery is .thin and its course slightly tortuous. The artery is not connected with the dorsal segmental arterial series or with any other artery. The further history of the external iliac is rather remarkable. It soon becomes quite straight and acquires a wall of great thickness, but remains unbranched until a stage of (approximately) 12 mm. externa appears as a thick-walled straight artery in the well- known pig embryo of 12 mm.


The place of origin of the a. iliaca externa marks the permanent subdivision of the dorsal root of the umbilical artery into two parts. The part becomes the adult a. iliaca communis while the distal part represents the a. hyjDogastrica and a short proximal section of its

al branch. At marginal vein is fully formed; its caudal

root, represented by the v. ischiadica, runs in close contact with the proximal of the corresponding artery


c. of 12 mm

M. E. C, no. H. 16, figs. 3 and 9 C

Condensation of the mesenchymal skeleton is now well advanced. It is not sufficiently definite in the tarsal region, however, for the determination of the course taken by the connection between the axial artery and the dorsal rete of the foot, surfaces of the growing nerves are considerably roughened by the beginning outgrowth of numerous branches^ many of which can be identified.


The course of the axial artery is somewhat less straight than in the preceding stage. This is due chiefly to a sharp convexity directed toward the growing extremity of the a. femoralis. The convexity is surmounted by a short sprout indicating the point


at w


the femoral is later to unite with

Although the axial artery is straighter in the

than at the stage of 12 mm., an irregularity is

preceding stage

at the

stage of 8.5 mm. in a similar situation. It seems to represent


an earlier indication of the convexity the present stage of dev Distal to the knee the between the tibia and

is so pronounced at

artery lies in the narrow interval The interosseous membrane and

muscles are still unrecognizable, but, although the ges toward the extensor region, its course


artery

clearly indicates that it does not leave the flexor aspect of the

Ipcr


proximal

econd bend

This bend is so pronounced as to practically amount to the bud of the vessel which is shortly to grow into the extensor aspect of the leg from this point.

The dorsal and plantar retia of the foot are richer than in the preceding stage. The connection between the axial artery and

the dorsal rete is r. perforans tarsi.


The a.

externa has


into the a. epigas

inferior and the a. femoralis.® The latter is contrasted sharply from the a. iliac externa by the thinness of its walls, which con- sist of endothelium only. Its structure resembles very closely that of the femoral vein which accompanies it. The

runs parallel with and upon the medial side of the n.

nus. Its extremity, now about half way along the femur, is bifurcated into a lateral and a medial branch. The former is

and will later join the axial artery; it may be called the


  • That the a. epigastrica inferior is an indejiendent branch of the a. iliaca externa, which considerably antedates it and the a. femoralis in has already been pointed out by the writer (Senior, '17).


ment,

ramus commumcans superius

The latter is

er

and

IS

recognizable as the ramus saphenus of the a. genu suprema.

The difficulty in finding developmental stages in which the a. femoralis is present, but not yet united with the axial artery, coupled with the thinness of the wall of the femoral artery at this stage, indicates that the artery is one of extremely rapid growth. In a 12-mm. embryo slightly younger than the specimen described (C. E. C, No. 3), reconstruction was begun under the impression that the femoral was absent. After more thorough study the artery was identified, bifurcated as in IVI. E. C, No. H 16, but much shorter. At this stage the a. femoralis has no branches, other than the terminal bifurcation already referred to.

m

d. Stage of I4 mm

C E. C, no. 5, figs. 4 o.nd 9 D

the a. femoralis in the blood

of the leg and by the

the two

appearance of three branches of the axial artery.

The r, communicans superius of the a, femoralis has joined axial artery at the more proximal noticed in the preceding stage.

can be traced to the level of t the more distal bend of tl

bend


The r. sa

remam

branch

proximal end

space and takes a recurrent course toward


The

proxim

formation

a. tibialis anterior.

may be referred to as the ramus cruris. The recurrent vessel continuing from the r. perforans cruris is the arteria recurrens tibialis anterior of the


The


k.


upon the axial artery by means of the r. and by the origin of the r. perforans

cruris, respectively, may be used tor tlie convenient subdivision of the vessel into three parts. The part upon the proximal side


of the r. communicans superius w

be

to as

a.

ischiadica and that upon the distal side of the r. perforans cruris

Senior1919 fig04.jpg

Fig. 4. Reconstruction showing the arteries of the right side of the pelvis and right thigh and leg in a human embyro, of 14 mm. (C.E.C., 5). X 20 diams.

Senior1919 fig05.jpg

Fig. 5. Reconstruction showing the arteries of the right side of the pelvis and right lower extremity in a human embryo of 17.6 mm. (H.E.C., 839). aspect. X 20 diams.

Senior1919 fig06.jpg

Fig. 6. Reconstruction showing the arteries of the right side of the pelvis and right lower extremity in a human embryo of 18 mm. (C.E.LC, 409) X 20 diams.


as the a. interossea- The intervening jDart will be called the a. poplitea profunda.

At this stage the a. poplitea profunda has two branches which course longitudinally through the posterior crural region. One of these resembles, in a general way, the a. tibialis posterior of the adult, it may be called the a. tibialis posterior superficialis.

The slightly more


in its place of


origin is the a, peronaea posterior superficialis (of HyrtVjJ The relations borne by these arteries to the n. tibialis remain constant throughout a prolonged period of development.

The a* tibialis posterior superficialis passes at first backward

side of the n. tibialis to reach its posterior aspect. Running upon the posterior aspect of the n. tibialis in the leg, it passes into the sole upon the inferior aspect of the n.


plantaris


t of the artery which enters the sole becomes the a. plantaris medialis of the adult.

The a. peronaea posterior superficialis passes from the to the lateral aspect of the n. tibialis by skirting around


proximal and


s of a large muscular ramus of the


nerve. It follows the anterior and lateral aspect of the n. tibialis as far as the place of origin of the nn. plantares. In this situation the artery bifurcates into a lateral and a medial The branches are both short and end blindly.


Two branches now spring from the lateral side of the a.

One of these is situated upon the proximal side of the r. saphenus and represents the r. musculo-articularis of the .adult a. genu suprema. The other is the a. circumflexa femoris lateralis of the adult a. profunda femoris.

The branches arising from the medial side of the a. femoralis which will be discussed under stages E and F.

The a. glutaea superior is present and takes origin from the

root of the a. ischiadica.


^ According to the system of nomenclature in use at the present time, the iective 'posterior' as used by Hyrtl is redundant. In view of the essentially


fugitive nature of anatomical terminology it has seemed unnecessary to modify Hyrtl's original term, which adequately meets the requirements of the case.

i musculares for the mm. popliteus,


s This is resolved later into the tibialis posterior, flexor digitorum longus, and flexor longus hallucis.


e. Stage of 17.8 mm

H. E. C.^ no. 839,^ figs. 5 and 9 E

During the iDreceding stages of develoi3ment the arterial retia of the foot have received their blood supplj^ exclusively through the a. interossea; the reta plantare directly, and the rete dorsale by means of the r. perforans tarsi. The mesenchymal skeleton of the foot is now definitely circumscribed, and it is plain that the latter vessel reaches the dorsum by way of the tarsal sinus. The arterial retia of the foot lie in close contact with the tarsus and metatarsus and represent the following vessels of the adult circulation — the arcus plantaris and its articular branches, the aa. tarseae mediales and laterales, the a. arcuata, the aa. metatarseae and digitales (both dorsal and plantar), and the rami perforantes (including the ramus plantaris profundus).


The present stage is characterized by the presence of four arteries which traverse the leg for the supply of the sole. The a. interossea is still present, the aa. tibialis posterior superficialis and peronaea posterior superficialis have formed their definitive connections, and a new vessel, the a. tibialis anterior, pars distalis, has arisen.


The a. tibialis posterior superficialis and the a. peronaea posterior superficialis preserve in the leg the same relations to the n. tibialis as obtained in the preceding stage. At the ankle the medial terminal branch of the a. peronaea posterior super- ficialis has traversed the fork formed by the diverging plantar nerves to join the a. tibialis posterior superficialis. The lateral terminal branch of the same artery has reached the lateral side of the sole to join the plantar arterial rete. The connection thus formed between the a. rete plantare becomes the a. plantaris lateralis of the adult foot. At the present stage of development it receives blood from two


  • The greatest total length of this embryo, measured in formalin, was 17.8 mm. In 80 per cent alcohol it measured 13.6 mm. It has been described by Thyng as a 17.8 mm. embryo (Am. Jour. Anat., vol, 17, p. 31), and referred to by Thyng (Am. Jour. Anat., vol. 7, p. 489) and hy Thyng and Lewis (Am. Jour. Anat., vol. 7, p. 505) as an embrj^o of 13.6 mm. The distribution of the arteries of the lower extremity resembles that of other embryos of about 15 or 16 mm.


The part of the a. tibiaus posterior superncialis distal to the origin of the a. plant aris lateraUs now the a. plantaris mediahs. The portion of the remainder of that, vessel which is not concerned in the formation of the a. poplitea. becomes the a. tibialis posterior.


The branches of the medial plantar artery anastomose, upon the lateral side of the foot, with the plantar rete, thus consti- tuting a (transitory) superficial plantar arch.


The a. tibialis anterior, pars distalis, extends from the part of r. perforans cruris which lies in the extensor region of the leg to the rete dorsale. The portion of the r. perforans which now lies beyond the proximal end of the pars distalis corresponds to the adult a. recurrens tibialis anterior. The portion which extends, from the a. poplitea profunda to the pars distalis enters into the composition of the adult a. tibialis anterior. The a. recurrens. tibialis anterior is connected by means of a plexiform anastomosis, with the r. saphenus of the a. femoralis.


Upon the medial side of the a. femoralis there are at this, stage three branches exclusive of the r. saphenus. Of these the most distal, which has a longer individual course than the others, takes a recurrent direction. The three branches break up to form an extensive plexus (not indicated in the figures) which ramifies throughout the thigh and is particularly rich around, the perichondrium. It is probable that this plexus is eventually taken over by the adult a. profunda femoris and its branches. Two branches arise from the lateral side of the a. femoralis as. in the preceding stage.

The a. glutaea superior now takes du-ect origin from the a. hypogastrica upon the proximal side of the origin of the a. ischiadica.


Stage of 18 mm

C. I. E. C, no. 409, figs. 6 and 9 F

From the time of the junction between the r, communicans

superius and the axial artery the caHber of the a. femoralis has

exceeded that of the a. ischiadica^ which has now become exceedingly slender. After having traversed the lower of the sacropudendal plexuS; the a. ischiadica passes.

to the region of the hiatus tendineus upon the lateral side of the n. tibiaUs. The n. peronaeus lies immediately upon its lateral


In a general way the aa. poplitea profunda and interossea and their branches have the same arrangement as in the preceding stage. The exact course taken by these vessels can now


ed, since it is possible to identifv the individual


muscles of the limb.

The a. poplitea profunda runs between the m. popliteus and

. At the proximal border of the muscle the artery gives off the a. genu media and a short trunk which is being formed by the progressive union of the proximal ends of the aa. tibialis posterior superficialis and the a. peronaea posterior super- ficialis. This short trunk, which lies upon the posterior surface of the m. popliteus, may now be called the a. poplitea super- ficialis. It forms the distal part of the a. poplitea of the adult. A short distance below the origin of the a, poplitea superficialis there arises the a. genu inferior medialis.

The a. interossea passes down the leg between the m. tibialis posterior and the interosseous membrane. Just above medial malleolus it gives off a branch which passes around the posterior to the medial side of the tibia, the ramus coronarius of the medial malleolus (Hyrtl).^^ At the malleolus the a.

  • In this vessel lies, according to Hyrtl, the key to the deep supramalleolar

anastomosis (i.e., the r. communicans) between the a. perong^ea and the a. tibialis posterior. The r. coronarius is regarded by Hyrtl as primarily passing from the a* peronaea around the medial side of the tibia to unite with the a. tibialis anterior. By means of a secondary connection occurring between the r. coronarius and the a. tibialis posterior, the former vessel eventually becomes converted into an anastomosing chain in which the aa. malleolaris anterior medialis, malleolaris posterior medialis and r. communicans are the named components. At the stage of 18 mm. of this series the r. coronarius arises from the part of the a. interossea which persists to take part in the formation of the adult a. peronaea. It runs, at this stage, as at the stage of 22 mm,, toward the a. tibialis anterior as described by Hyrtl, and would, no doubt, eventually join it. Since in both these stages the a. tibialis posterior is situated upon a plane superficial to that occupied by the r. coronarius, no junction of the vessels in question has occurred. There can be little doubt, however, that Hyrtl has interpreted the nature of the r. coronarius correctly. His views upon this subject, which were derived from an extensive study of the normal and abnormal conditions found in adult legs, have been of the greatest assistance in the interpretation of the conditions obtaining during development.


interossea lies upon the lateral side of the tendon of the m. tibialis posterior (i.e., between tendon and malleolus) and then passes across the plantar end of the sinus tarsi to join the plantar

rete.

The a. peronaea posi^erior superficialis is placed anteriorly and laterally to the n. tibialis and lies upon the posterior surface of the m. flexor hallucis longus. At the distal border of the muscle the artery lies near the a. interossea and interosseous membrane. In this situation it gives off a very large r. calcaneus lateralis which runs upon the lateral side of the tuber calcanei. This branch eventually forms the termination of the a. peronaea.


The a. tibialis posterior superficialis follows the posterior surface of the n. tibialis until the latter bifurcates in the neighborhood of the medial malleolus. Here the artery is placed between the n. tibialis and the tendon of the flexor hallucis longus. The a. tibialis anterior, pars distalis, has relations identical with those of the adult.


The relations existing between the various structures of the leg were ascertained by making a reconstruction which, from the fact that it yields but little information when entirely built


up, IS uns



The data gained from an examination of its separate parts are embodied in two diagrams (fig 7, A and B) which may serve as a rough guide to the inter- pretation of anomalies. These diagrams show, approximately, the course taken by the embryonic aa. poplitea profunda,


interossea, and peronaea posterior superficialis.

The order in which the various structures passing from the leg to foot are arranged in the hollow between the medial mal- leolus and tuber calcanei is as follows: m. tibialis anterior and a. interosseus together: m. flexor digitorum longus; a. peronaea


posterior superficialis; n. tibialis, a. tibialis posterior super- ficialis, and m. flexor hallucis longus.

Embryos of about this age are instructive mainly by reason of the fortunate circumstance that the individual muscles are


differentiated before the continuity of the axial artery has been broken. Only one important change has occurred at this stage of development; this consists in the appearance of a communicating branch which foreshadows the development of the

^e a. peronaea.

. The communicating branch in question leaves the a, peronaea posterior superficialis at the proximal border of the m. flexor

gus. It passes distally between the mm. flexor hallucis longus and tibialis posterior to join the a. interossea, as that artery lies upon the interosseous membrane. It may be called the r. communicans inferius.


Senior1919 fig07.jpg

Fig, 7. Indicates the course of three arteries of the embryonic lower extremity, represented diagrammatically as they would appear if persisting in the adult. The vessels which normally persist are indicated by shading. A, A. poplitea profunda and a. interossea. B. A. peronaea posterior superficialis. d. L m. flexor digitorum longus; h, L, m. flexor hallucis longus; L p., m. tibialis posterior.



The entire r. communicans inferius persists in the adult as the portion of the a, peronaea which lies between the mm. flexor hallucis longus and tibialis posterior. The portions of the aa. peronaea posterior superficialis and interossea with which the


and distal ends of the r. communicans inferior are


connected


a* peronaea.


Of the branches of the a* femorahs^ those arising from the

lateral side are identical with the branches of the preceding stage. There are three branches upon the medial side, recurrent branch {R in figures) seems to be identical with the



similar branch of the preceding stage. It is doubtful whether the two other medial branches correspond to those observed in the preceding stage or not.


g. Stage of 22 mm

C /. C no. 1, figs. 8 and 9 G


At this stage of development the continuity of the a. ischiadica has been interrupted and the a. femoralis alone conveys blood to the region beyond the knee.

The femoral artery pursues a more direct course than before and gives origin to most of its important branches. In addition to the a. circumflexa lateralis which appeared at the stage of 14 mm., it gives origin to the a. pudenda externa and the a. profunda. The r. musculo-articularis has migrated to the em-




nic r. saphenus. The root of the latter branch, now appears as the a. genu suprema and gives origin to the r. saphenus and the rr. muscularis and articulares of the adult.

The a. profunda arises from the a. femoralis quite close to the origin of the a. circumflexa lateralis. It seems probable that

onic a. profunda sometimes arises from the root of the latter artery and sometimes directly from the femoral. In the former case the adult a. circumflexa lateralis would appear to arise from the a. profunda and in the latter from the femoral. The great variation in the site of the origin of the vessel is well known.

The a. profunda femoris gives origin to one perforating artery y since it pierces the adductores brevis and magus, repre- sents the first or second of the adult series. The single a. per- forans is connected, by means of an extensive plexus, with the more distal section of the now interrupted a. ischiadica.


The a. ischiadica passes through the sacropudendal j^lexus as before and reaches the lateral side of the a. tibialis, which is now contained in the same sheath as the n. peronaeus. After its exit from the pelvis the artery gives origin to a few gluteral branches and leaves the n. tibialis with the n. cutaneus femoris posterior. In company with the latter nerve and the v. ischiadica, it passes to the posterior surface of the thigh and ends dividing into several cutaneous branches. This part of the a. ischiadica persists as the a. glutaea inferior.

The more distal portion of the a. ischiadica is traceable as a definite path through a plexus upon the posterior surface of the m. adductor magnus, but has lost its continuity wdth the a.



pophtea. The other vessel participating in the


of


the plexus is the perforating branch of the a. profunda femoris. This plexus evidently represents the terminal anastomosis between the perforating arteries of the adult. It probably takes a large share in the formation of the perforating arteries themselves.

The distal part of the anterior tibial artery has received blood since the time of its first appearance by way of the a. poplitea profunda and r. perforans cruris. An alternative path has now

by the appearance of a vessel which, passing

of the m. popliteus, connects the

around

distal

developing a. peronaea with a more distal part of the a. poplitea profunda. It is the r. communicans medius which will later become the definitive proximal end of the a. tibialis anterior. The significance of this vessel in relation to the formation of the adult aa. profunda and tibialis anterior will be dealt with in the succeeding section.

The principal changes which have occurred in the embryonic arteries of the posterior crural region since the preceding stage

participate in the

of development involve the vessels

formation of the adult a, peronaea- These changes cons' st in the disappearance of considerable parts of the aa, interossea and peronaea posterior superficialis.

The portion of the a. interossea which formerly extended from the r. perforans cruris. to the distal end of the r. communicans

Senior1919 fig07.jpg

Fig. 8. Reconstruction showing the arteries of the right side of the pelvis and right lower extremity in a human embryo of 22 mm. (C.E.I.C, 1.). Medial aspect. X 20 diams.

inferius has practically disappeared. The portion immediately beyond the distal end of the latter vessel lies upon the posterior surface of the interosseus membrane and gives origin to two branches. The remainder of the vessel is involved in the meshes of the rete calcaneum.

The portion of the a. peronaea posterior superficialis which extends from the present termination of the a. popUtea super- ficialis to the proximal end of the r.


commumcan

sists the re


of the

become a part of the adult a. peronaea. ainder of the artery has been lost, but th essel can still be recognized as forming a

aspect of the rete calcaneum. Thi

A large part of artery can be traced through the meshes of the rete as far as

the a.

The rete calcaneum is very

ive at this stage of develop

ment and occuT^ies the concavity upon the medial side of the

surrounds the

m


the


malleolar region of the leg.

The component parts of the a. peronaea are now recognizable. The proximal part is derived from the a. peronaea posterior super-

hallucis longiis and

The

between tibialis posterior represents the entire r. communicans inferius. The immediately succeeding part, which rests upon the mem- brana interossea, is derived from the a. interossea. The terminal part of the artery consists i the a. peronaea posterior su of the r. calcaneus lateraUs of . The connection between

the a. interossea and the part of the latter artery which gives origin to the calcanean branch is effected through the agency of


the plexus calcaneum.

The part of the a. interossea which takes part in the formation of the a. peronaea has been noted as giving rise to a branch, the r. coronarius, at the stage of 18 mm. At the present stage another branch arises from it, namely, the r. perforans. Both


of them become branches of the adult artery. At the stage of 22 mm. the r. coronarius can be traced around the posterior and medial aspects of the tibia almost as far as the a^ tibialis anterior. The views expressed by Hyrtl upon the conversion


Fig. 9 Reconstructions showing the arteries of the right lower extremity in the seven human embryos shown in the preceding figures. Tlie cephalic (embryonic pre-axial, adult medial) aspect is shown in all cases. A, X 40, the others X 20 diams. The skeleton is shown, in part, in E, F and G. Parts of the tibia


a femon a. eplgast. inf.


r. SQphtn.


n SGphen,


I: com. sup. n. obtur.

r. perf, tarsj retc


a pudend int

n, tiblol


C /2 n7An.


and tarsus are omitted in E, the tibia in F and the tibia and medial femoral condyle in G. The fibula is omitted in all. The medial plantar artery has been almost entirely removed from E and F. In C, a. femor. should read a. iliaca ext.


of the r. coronarius into the communicating branch and medial malleolar arteries of the adult have been noted above (footnote 10, p. 73). A small


of

a. peronaea posterior super



I

appears at the present stage as a branch of the a. peronaea. It runs upon the posterior surface of the m. flexor hallucis longus. The disintegrating a. interossea has left a similar vestige of its


'osseous


proximal end upon the posterior surface of its membrane. This vestigial branch occasionally persists as a branch of the adult a. tibialis anterior.^^ The terminal part of the main trunk of the a. peronaea posterior superficialis is now involved in the rete calcaneum. It usually leaves its mark in the adult as a recurrent element among the leash of known as the r. calcaneus medialis of the a. plantaris


The aa. iliolumbalis

sacralis lateralis now arise from



a. elutaea



The root of the latter artery has conse-


quently become the



division of the



a. hypo-


gastrica. All the visceral arteries of the pelvis, with the

their



of the a. vesicalis superior, have



relations


h. Changes occurring in the principal arteries subsequent to stage of 22 mm .


A. Formation of the adult a. poplitea and a. tibialis anterior.


Fig. 10, A, C. I. E. C, 22; B, C E. C, 1; C, C. I. E. C, 840.

The r. communicans medius, the presence of which was noted at the stage of 22 mm., seems to arise at about that stage of

In C. E. C, no 1, it is larger upon the right side than upon the left and in C. E. C , no. 6, which also measures 22 mm., it is absent altogether.



  • ^ Mr. Kimbrig has kindly dissected six adult legs for evidence of persistence

of this vessel. In two instances he found a branch accompanying the n. interos- seus cruris for a short distance. In both cases the branch arose from the root of the ramus fibularis.

It is very questionable whether the B. N. A. is correct in classifying the r. fibularis as belonging to the a. tibialis posterior. It has usually been regarded, in English-speaking countries at all events, as a branch of the a. tibialis anterior.


At the stage of 20 mm. (fig. 10, A) blood traverses the popliteal region to reach the r. perforans cruris through the original channel, namely the a. poplitea profunda. The a. poplitea is longer than at the stage of 18 mm., having increased in length at the expense of the aa. tibialis posterior and peronaea posterior superficialis. At the stage of 22 mm. (fig. 10, B), a junction between the developing a. peronaea and the distal part of the a. poplitea


Senior1919 fig10.jpg

Fig. 10. Three reconstructions, each showing a sagittal segment (0.25 mm. thick) from the left leg of an embryo of the length indicated. Lateral aspect. X 19. A, 20 mm. ; B, 22 mm. ; C, 24.8 mm. The tibia appears in all cases. P. indicates the position of the m. popliteus. c. m., a. communicans media; g, i. m., a. genu inferior medialis; g, m., a. genu media; i., a. interossea; {. m., interosseous membrane; p., a. poplitea; p. c, a. perforans cruris; p- d.^ a. tibialis anterior, pars distalis; p. p., a. poplitea profunda; p. s., a. poplitea superficialis; per., a. peronaea; r. a,, a. recurrens tibialis anterior; r. p., a. recurrens tibialis posterior; t, a., a. tibialis anterior; t, p. s., a. tibialis posterior superficialis.


profunda has been effected by the development of the r. com municans medius. Blood may now pass from the proximal par of the a. poplitea profunda to the a. tibialis anterior, pars distalis by super



routes: 1) anterior to the m. popliteus, by way of the a. poplitea profunda and r. perforans cru or to the m. popliteus, by way of the a. poph developing a. peronaea, r. communicans medius


poplitea profunda, and r. perforans cruris.


At the stage of 24.5 mm. (fig. 10, C) upon the anterior surface of the m.


ect

s

route

to

exist. The part of the a, pophtea profunda not incorporated in

the definitive a, poplitea or


anterior is represented :

1) by the root and a small branch of the a. genu inferior medialis of the former and 2) by the a. recurrens tibialis posterior of the latter. The main arterial channel through the popliteal region has thus been transferred from the anterior to the posterior surface of the popliteus muscle. Both the a. poplitea and the a. tibialis anterior have assumed their adult arrangement.

The formation of the adult a. poplitea results from the combination of two embryonic elements. The part of the vessel which extends from the hiatus tendineus to the origin of the a. genu inferior medialis is derived from the embryonic a. poplitea profunda. The remainder of the artery corresponds to the embryonic a poplitea superficialis.

The embryonic components of the a. tibialis anterior consist of the r. communicans medius, a short section of the distal end of the a. poplitea profunda, the proximal part of the r. perforans cruris, and the entire tibialis anterior, pars distalis.

The a. poplitea superficialis reaches' completion at the stage of 24.5 mm. by extending as far as the r. communicans medius becomes one of branches.


means the a. peronaea rehnquishes its temporary in the formation of the a. tibialis anterior.


this


ion

B. The conversion of the

yonic a.

s posterior super

ficiahs into the adult a. tibialis posterior.


a. tibialis posterior superficialis is originally a branch of the a. poplitea profunda and extends into the sole. The distal portion of the artery, marked off from the remainder of the vessel upon the development of the a. plantaris lateralis, becomes the a. plantaris medialis. The proximal portion of the a. tibialis posterior superficialis has blended with the corresponding section of the a. peronaea posterior superficialis at the stage of 24.5 mm. as far as the termination of the popliteal artery. The further blending between these two arteries which is to occur during the later stages of development will cause the migration of the


origin of the a. peroiiaea from the termination of the a. poplitea

tibiali;


com


pleted by the occurrence of these changes the vessel still retains its orig

to


n. The relations between


the


The



a, poplitea lies upon the


side of the n. side of the tibialis. The a. tibialis posterior crosses the

nerve to gain its posterior aspect upon which it runs until it

ends behind the

malleolus. The relations of the aa.

itea and tibialis posterior to the n. tibialis have been

tudied UD to the stage of 22 mm

eem

remain unaltered m the olde been examined in this regard, measures 33.5 nmi.

embryo which has C no. 1134, Tvhich


It is not difficult to see how an agency capable of moving the termination of the a. poplitea across the anterior aspect of the n. tibialis from the medial to the lateral side would produce a condition differing little from that normally encountered in the adult. Since the knee is flexed throughout intrauterine life it would seem that the modification of the relative positions of the arteries and nerve might depend upon the straightening of the n. tibiahs which occurs at birth. In order to put the matter to the test, a foetus of 7.9 cm. was dissected. ^^ The relations, however, were found to be identical with those of the adult.

Apart from the study of a few special points, this investigation has not extended beyond the stage of 22 mm. At that period all the vessels of the adult limb are present with the exception of two of the three aa. perforantes, which usually arise from the adult a. profunda femoris, the a. circumflexa femoris medialis, and the a. obturatoria. At the stage of 22 mm. two obturator veins are present in C. E. C, no. 1, one of these is tributary

V. hypogastrica, the other to the v. femoralis.

The leading features in the process of the arterial development of the limb are indicated in figure 11.

^2 For this dissection and for many others made upon various mammals, I wish to express my indebtedness to Mr. B. Spector.

III. Brief Developmental History Of The Individual Arteries

A. Axis. This artery is a branch of the dorsal root of the a. umbilicalis, its presence has been noted by Tandler as early as the stage of 5 mm. '03). At the stage of 6 mm. it terminates by giving origin to the r. perforans tarsi and to the rete plantare.


The axial artery has three rami communicantes, and gives origin to three rami perforantes as follows:

The r. communicans superius, from the a. femoralis, joins it near the hiatus tendineus shortly before the stage of 14 mm.

The r. communicans medius^ from its own branch the a. peronaea posterior superficiaHs, has joined it near the distal border of the m. popliteus at the stage of 22 mm.

The r. communicans inferius^ from the a. peronaea posterior superficialis, joins it, near the distal border of the m. posterior, between the stages of 17 and 18 mm.

The r. perforans cruris arises between the stages of 13 and 14 mm.

The r. perforans arteriae peronaea arises between the stages of 18 and 22 mm.

The r. perforans tarsio is present at the earliest stages of development at which the axial artery has been observed.

Two points have been marked upon the axial artery at the stage of 14 mm. which may be used for the convenient sub- division of the axial artery into three parts. These points correspond to the termination of the r. communicans superius and to the origin of the r. perforans cruris, respectively.

The respective parts of the artery are defined and named as follows: The part upon the proximal side of the termination of the r. communicans superius is the a. ischiadica, while that upon the distal side, of the origin of the r. perforans cruris is the a. interossea. That part intervening between the other two is the a. poplitea profunda. Further information regarding the axial artery may be found under the headings devoted to the description of its respective parts.

A. dor salts pedis. This artery is a channel through the embryonic rete dorsale. Its importance dates from the appearance


Fig. 11 Diagram to illustrate the general development of the arteries of the human lower extremity. Adult arteries are stippled and their names underlined. The chief embryonic channels are outlined in black. The black line is continuous only in the case of the axial artery, otherwise it is broken. The letter P indicates the position of the m, popliteus; T, that of the m. tibialis posterior, and H that of the m. flexor hallucis longus.


of the distal part of the a. tibiahs anterior Which is developed between the stages of 15 and 16 mm.

Branches. One of the adult rr. tarseae laterales represents

5al end of the r. from the rete dor,

other branches are


A. femoralis. This artery arises from the a.

externa

between the stages of 11 and 12 mm. From the time of the first appearance of the femoral artery its growing end is bifurcated into the r. communicans superius and the r. saphenus. The r, communicans superius traverses the hiatus tendineus and joins the a. axis between the stages of 12 and 14 mm., while the r. saphenus terminates below the region of the knee-joint.

Branches. The A. profunda femoris seems to be derived from an arterial plexus which envelops the femur as early as the stage of 14 mm. The proximal end of the artery is distinguishable at the stage of 22 mm. The a. circumflexa lateralis arises from the femoral trunk shortly before the stage of 14 mm. artery is commonly regarded as a branch of the a. profunda, its original connection with the a. femoralis is frequently retained in the adult. The a. circumflexa medialis is not present at the stage of 22 mm. One of the a. perforantes, the first or second, is present at the stage of 22 mm., and is involved at that period

Although this

of development in an extensive arterial plexus connected with the remainder of the distal part of the a. ischiadica. The other perforating arteries are not present, at the stage of 22 mm.

The

a. pudenda externa is the only superficial inguinal branch present at the stage of 22 mm. The a. genu suprema corresponds to

a

the part of the r. saphenus upon the proximal side of the origin of the rr. musculares and articulares. These branches arise



from the a. femoralis, but have migrated to the embryonic r. saphenus by the stage of 22 mm. The distal portion

of the

xL m


vessel corresponds to the r. saphenus of the adult. strica. The main stem of this artery represents the

part of the dorsal root of the a. umbilicalis which lies beyond the place of origin of the a. iliaca externa.

Branches. The


ior division of the a. hypogastrica is derived from the proximal part of the a. axis, which becomes the

denda


a. glutaea inferior, from the root of from the part of the a. umbilicalis dorsal root. The portion of the contributes to the formation of the a. hypogastrica is the source, in all probabiHty, of all the visceral branches of the artery. The a. obtoratoria is not present at the stage of 22 mm. In consequence of the transference of the origins of the aa. iliolumbalis and sacralis lateralis to the a. glutaea superior, part of that artery becomes the posterior division hypogastrica.

4. iliaca communis. This artery is derived from the portion

of the dorsal root of the a.

lies upon. proximal side of the origin of the a. iliaca externa.

A. iliaca externa. This artery already springs from the con- vexity of the a. ihaca communis at the stage of 8.5 mm. Its termination is unbranched until a period shortly before the stage of 12 mm., when it divides into the a. epigastrica inferior and


the a. femoralis


The a.


arise


from the a. iUaca externa between the stages of 18 and 22 mm.


A. interossea. The course of this part of the axial artery is described on page 73,

The a. interossea is joined before the stage of 18 mm. by the distal end of the r. communicans inferius. The junction occurs at a point immediately beyond the inferior margin of the m.

m

s posterior. This artery has given origin to the r. coronarius at the stage of 18 mm. and to the r. perforans and to branch of communication with the a. peronaea posterior superficialis at the stage of 22 mm.

The part of the a. interossea extending from the termination of the a. popUtea profunda to the distal end of the r. communicans disappears between the


ges of 18 and 22 mm. A


vestige of the proximal end of this part of the artery sometimes persists in the form of a small branch of the a. tibialis anterior or of the r. fibularis.

The small portion of the a. interossea which extends from the distal end of the r. communicans inferius to that of the membrana interossea persists as the third part of the a. peronaea (p. 79).


which arise from this portion of the a. interossea are transferred

They are the r. coronarius

r. communicans,


and the r. perforans. The remainder of the a, interossea has lost its identity at the stage of 22 mm. The r. perforans tarsi disappears at about the same period.


A. ischiadica. The course taken by this part of the artery is described on page 73.

The continuity of the a. ischiadica has been broken in the region of the glutaeal fold^ at the stage of 22 mm. The proximal part of the vessel, which has now become the a. glutaea inferior,

to the


follows the V. ischiadica and the n. surface of the limb where it ends by dividing into cutaneous branches. The more distal portion of the artery is involved, with the single perforating artery present at the stage of 22 mm., in the formation of an extensive plexus upon the posterior surface of the m. adductor niagnus.

A. peronaea. This artery is clearly recognizable at the stage of 22 mm. (p. 79). It may be divided into four parts:

The first part of the a. peronaea, which extends from the origin of the artery to the proximal margin of the m. flexor hallucis longus, is a persisting portion of the a. peronaea posterior superficialis (p. 74).

The second part, which lies between the m. tibialis posterior and the m. flexor hallucis longus, represents the entire embryonic r. communicans inferius (p. 76).

The third part, which is short and rests upon the interosseus membrane near the distal border of the m. tibialis posterior, is R persisting portion of the a. interossea (p. 73).

The fourth part, which ramifies upon the fibula and calcaneum in the neighborhood of the lateral malleolus, represents a survival of the short portion of the a. peronaea posterior super-

and of the entire r. calcaneus lateralis of that vessel

(p. 74).


r, perforans and r. communicans, belong

originally to the a. interossea. The rr. calcanei laterales are branches of the r. calcaneus lateralis of the a. peronaea posterior superficialis.


A. peronaea posterior



The course of this embryonic artery is described on pages 70 and 74.

of the vessel is present at the stage of 14 mm.^ its terminal branches form their definitive connections at a stage of 15 or 16 mm.

The proximal part of the a. unites with the a. tibiahs posterior s

pophtea


and the part of


erior superficialis is to form the a.

posterior

above the root of the a. peronaea. A more distal portion persists as the first part of the a. peronaea^ and a still more distal portion enters slightly into the formation of the fourth part of that

vessel.


The terminal of the a. peronaea posterior superficialis form the adult a. plantaris lateralis. The r. calcaneus medialis of the latter artery represents the end of the stem of the parent vessel. The r. calcaneus lateralis, which arises from the a. peronaea posterior superficialis shortly before the stage of 18 mm., persists to form the major portion of the fourth part of the a. peronaea (p. 79). A. plantaris


The part of this artery represents the medial terminal branch of the a. peronaea pos-

71), which unites with the a. posterior superficialis. The distal part represents the lateral terminal part of the same vessel.

Branches. The r. calcaneus mediahs represents the terminal portion of the main trunk of the embrj^onic a. peronaea posterior superficiaHs. The arcus plantaris and all its branches are de- rived from the embryonic rete plantare.

A. plantaris medialis. This artery is the distal portion of the


'^omc a.

posterior

It is

off from the remainder of that vessel by the medial terminal branch of the embryonic a. peronaea posterior superficialis.

A. poplitea. The part of this artery above the origin of the a.

genu


a surviving portion of the

embryonic a. poplitea profunda (p. 73). The part Ij^ing upon the posterior surface of that muscle represents the embryonic a.

popHtea


The proxi


of

a. genu

inferior mediahs is derived from the a. poplitea profunda.

Branches. The a. genu media is present at the stage of 18 mm. The other branches appear at a later stage of the development.

. poplitea projimda. The course of this vessel is described on page 73. The part of the a. pojDhtea i3rofunda which from the hiatus tendineus to the origin of the a. genu


me


the part of the adult a. poplitea.

The remainder of the artery is represented in part by the root of the a. genu inferior medialis. It is represented also by the a. recurrens tibialis posterior and by the second part of the a. tibialis anterior (p. 84).

A. poplitea superficialis . The formation of this artery results from the gradual union which takes place between the proximal part of the embryonic a. tibialis posterior superficialis and that of the a. peronaea posterior superficialis. The vessel lies upon the posterior surface of the m. popliteus and has nearly reached completion at the stage of 22 mm. The a. poplitea superficialis persists as the distal portion of the adult a., poplitea (p. 84).


anterior. This vessel may be divided into


parts which correspond the adult artery.


the four embryonic components of

The first part extends from the origin of the vessel to the root

of the a. recurrens

posterior. It corresponds to the

whole of the r. communicans medius (p. 84).

The second part occupies the immediate neighborhood of the origin of the a. recurrens tibialis posterior. It represents, like that artery, a persisting portion of the embryonic a. poplitea profunda (p. 84).

The third part extends from the a. redurrens tibialis posterior

to a

beyond the root of the a. recurrens anterior. It is derived from the proximal portion of embryonic r. perforans cruris (p. 68). *

fourth part of the artery extends from the termination of the third part to the proximal end of the a. dorsalis pedis. It


represents embryo (p. 72).

entire a.

anterior, pars distalis, of the


Branches. The a. recurrens tibialis anterior represents the terminal portion of the a. perforans cruris (p. 68).

The a. malleolaris anterior medialis is derived from the r, coronarius of the a, interossea \Yhich arises shortly before the stage of 18 mm.


A. tibialis anterior, pars distalis. This embryonic artery arises at about the stage of 15 or 16 mm. Its course is identical with that of the fourth part of the a, tibialis anterior of the

A. tibialis posterior. The part of this artery proximal to the origin of the a. peronaea is the product of the union between the


a, tibialis posterior superficiahs and the a. peronaea posterior

The remainder of the vessel is a survival of the part of the stem of the a. tibialis posterior superficialis pr to the point at which it is joined by the medial terminal branch of the a. peronaea posterior superficiahs.

Branches. The a. peronaea is described on page 90- The

r. communicans are

a. malleolaris posterior derived from the embryonic r. coronarius malleolaris medialis of the a. interossea (p. 73).

A. tibialis posterior super ficialis . The course of this artery, which arises shortly before the stage of 14 mm., is described on page 70.

The whole of the a. tibialis posterior superficiahs persists in the adult hfe. In combination with the a. peronaea posterior superficiahs, the more proximal part of the artery forms the part of the a. poplitea in contact with the m. popliteus and the part of the a. tibialis posterior proximal to the origin of the a. peronaea.* The more* distal part of the artery persists as the portion of the a. tibialis posterior beyond the origin of the a. peronaea and as the a. plant aria medialis.

The relation of the part of the a. tibialis posterior superficiahs which forms the a. tibialis posterior of the adult to the n. tibialis is discussed on page 84.

Rete dorsale. The dorsal rete of the embryonic arises from the r. perforans tarsi. It forms all the arteries which are distributed upon the dorsum of the adult foot.


Rete plantare. This embryonic plexus arises from the terminal branches of the a. interossea. It furnishes the arcus plantaris and all the other arteries of the adult sole excepting the aa plantares.


  1. In the case of the embryos from the Carnegie Institution and Minnesota University the measurement is crown-rump. The Harvard and Cornell measurements represent the greatest total length.
  2. Ramus and sinum tarsi, Hyrtl ('64); Arteria tarsea perforans, Stissdorf ('89); perforans tarsi, DeVriese C92) Arteria anastomotica tarsi, Salvi ('99).
  3. The distinction between the respective origins of the visceral and parietal branches of the a. hypogastrica has already been pointed out by McMurrich ('04).
  4. It is questionable whether the common iliac artery should be regarded as belonging to the fifth lumbar dorsal segmental or not. At the stage of 8.5 mm. of this series the fifth lumbar segmental has regained its independence, and springs from the aorta (on both sides) between the fourth and fifth. The work of Levy ('02) shows, however, that absence of the a. lumbalis ima is the rule rather than the exception. Whether this vessel is frequently retained by the root of the a. iliaca commimis or merely overshadowed (as it were) by it is doubtful.

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