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

THE DEVELOPMENT OF THE ARTERIES OF THE HUMAN LOWER EXTREMITY

H. D. SENIOR

Deparlment 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 normally 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 (secondary) 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 traverses 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

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56 H. D. SENIOK

all mammalian forms is a question to which 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 b^ 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 human 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.

The 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 chief 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.

ARTERIES OF HUMAN LOWER EXTREMITY 57

Hochstetter did not succeed in following the continuation of the a. ischiadica 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. ischiadica of the rabbit as traversing the flexor region of the leg and dividing 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 cat and rabbit embryos and made considerable progress in the nomenclature to the primitive artery of the limb.

In Zuckerkandl' s second paper a distinction was made between the terms axial and ischiadic which formerly had been used more or less interchangeably to denote the primitive artery of the limb. For the entire artery Zuckerkandl employed the name axial. He restricted the use of the term ischiadic to the part of it which traverses the thigh 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 DeVriese, in 1902, described the a, interossea (the a. nervi interossei cruris of the latter author) in bat and human embryos, respectively, as pursuing the course it had been described by Zuckerkandl as following in the rabbit. Both of these observers also recorded the presence, in the 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 arter}^ has been tacitly included as a part of the a. ischiadica or not, since the distal limit of the latter artery does not appear to have been definitely fixed. In

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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. This 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. interossea 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. poplitea, 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 profunda 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.^

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.

1 Arteria ■poplitea. Ein Stuck dieser Arterie lagert bei den Halbaffen und den Primaten auf der freien (dorsalen) Flache des Musculus popliteus, bei den iibrigen Saugetieren auf der Gelenkskapsel, bedekt von dem oben erwahnten Muskel. Diese Verschiedenheit im Verlaufe der Poplitea kann nur auf die weise erklart werden, dass entweder die den Muskel querenden Stiicke der Poplitea nieht homolog Oder die beiden Muskeln nicht dieselben sind. Nach meinen bisherigen Erfahrungen scheint ersteres wahrscheinlicher zu sein. (Zuckerkandl ('95), p. 255.)

ARTERIES OF HUMAN LOWER EXTREMITY 59

The literature dealing with the arteries of the mammahan 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 relationship 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 Zuckerkandl's 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 w^hich 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 human 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 this manuscript.

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b. Material

In the present investigation the lower extremities of embryos have been studied in seven stages of developinent, one extremity or both having been reconstructed in wax. The selection of stages depended upon the accessibility of well-preserved material rather than upon a preconceived plan regarding the most instructive stages to use. 2

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

6.0 mm.* Carnegie Institution, Embryolugical Collection (C.I.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. 17.8 (?) 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.

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. Htockard, 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 made 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

2 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.

ARTERIES OF HUMAN LOWER EXTREMITY 61

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 n). 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 mammalian embryos hitherto observed, numerous terms have been applied. ^ 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.

^ Ramus and sinum tarsi, Hyrtl ('64) ; Arteria tarsea perforans, Siissdorf ('89); perforans tarsi, DeVriese ('92) Arteria anastomotica tarsi, Salvi ('99).

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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, wdth the exception of the fifth lumbar and second sacral, pass directly to the spinal cord without branching. The umbilical arteries, the ventral roots of w^hich are still very large, arise opposite the intervals between the third and fourth lumbar segmentals.

The secondary, or dorsal, roots of the umbilical 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 the fifth lumbar segmental artery a short distance beyond its root. The vessel in question is joined almost perpendicularly near its origin by a smaller one which springs from the aorta in the interval between the fourth and fifth lumbar segmental arteries.

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The dorsal root of the a. umbihcahs, 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 ventrally, passing upon the lateral side of the duct, which is now enclosed between the two roots of the umbilical artery, to join the ventral root.

As the dorsal root of the a. umbilicalis 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 tow^ards the surface. It ends by dividing into two

plex. obdom. O. umbil. phx. pelv. a. a^i's

0. pudend.

-/_. 1.

S.z

a. umbilic. radix ^ent. radiy dorsalis

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.

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. In addition to the arteries already described, there are two extensive arterial plexuses, which may be called the abdominal and 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 AMERICAN JOURNAL OF ANATOMY, VOL. 25, NO. 1

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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 pelvic plexus arises by two roots from the convexity of the umbilical artery opposite the roots of the abdominal plexus. 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 lateral 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 parietal 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.^

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. Stnge 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 and now spring from the aorta in the intervals between the fourth and fifth dorsal pairs of lumbar segmental arteries.^ The

The distinction between the respective origins of the visceral and parietal branches of the a. hypogastrica has already been pointed out by McMurrich ('04).

^ 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 communis or merely overshadowed (as it were) by it is doubtful.

ARTERIES OF HUMAN LOWER EXTREMITY

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jBfth 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 arterj-^ passes distally into the lower hmb, 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

o hypog rr perfor. tarsi.

a axis.

a. iliac, ext. n genitof^m. j a. iliac, com. n femor \

rete dorsal: rete p/ant.-^ n. perori, a pudcnd int

a. femor r sap hen. a. axis. r. com. sup.r perf. tarsi, rete dorsal.

n. peron.

a. hypoq.

T.i.r

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.

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

the extremities of the plantar nerves. Just as it is breaking up into the plantar plexus the axial artery gives origin to two or three branches which pierce the mesenchymal skeleton of the foot to reach the dorsum. Upon the dorsum of the foot the perforating branches produce 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.

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In passing from the medial to the lateral side of the sacropudendal plexus, the axial artery runs between the main plexus and a branch from its lower part. The branch referred to has been removed from the reconstructions illustrated in figures 1 to 6, since it partially covers the artery when viewed from the medial side.

From the lateral 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 ihac 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. The a. iliaca externa appears as a thick-walled straight artery in the wellknown 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 proximal part becomes the adult a. iliaca communis while the distal part represents the a. hypogastrica and a short proximal section of its umbilical branch.

At this stage the marginal vein is fully formed; its caudal root, represented by the v. ischiadica, runs in close contact with the proximal part of the corresponding artery.

c. Stage 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. The surfaces of the growing nerves are considerably roughened by the beginning outgrowth of numerous branches, many of which can be identified.

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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 which the femoral is later to unite with the axial artery. Although the axial artery is straighter in the preceding stage than at the stage of 12 mm., an irreg-ularity is noticeable at the stage of 8.5 mm. in a similar situation. It seems to represent an earlier indication of the convexity which is so pronounced at the present stage of development.

Distal to the knee the axial artery lies in the narrow interval between the tibia and fibula. The interosseous membrane and individual muscles are still unrecognizable, but, although the artery bulges toward the extensor region, its distal course clearly indicates that it does not leave the flexor aspect of the leg.

At what appears to be the proximal end of the very short tibiofibular interspace a second bend occurs in the axial artery. 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 now reduced to a single vessel of large size, the r. perforans tarsi.

The a. iliaca externa has bifurcated into the a. epigastrica inferior and the a. femoralis.^ The latter is contrasted sharply from the a. iliac externa by the thinness of its walls, which consist of endothelium only. Its structure resembles very closely that of the femoral vein which accompanies it. The femoral artery runs parallel with and upon the medial side of the n. saphenus. Its extremity, now about half way along the femur, is bifurcated into a lateral and a medial branch. The former is short and will later join the axial artery; it may be called the

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

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ramus communicans superius. The latter is longer 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 M. 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.

d. Stage of 14 mm. C. E. C., no. 5, figs. 4 and 9 D

This stage is principally characterized by the participation of the a. femorahs in the blood supply of the leg and by the appearance of three branches of the axial artery.

The r. communicans superius of the a. femoralis has joined the axial artery at the more proximal, of the two angular bends noticed in the preceding stage. The r. saphenus remains free and can be traced to the level of the knee joint.

At the more distal bend of the axial artery there is now a branch, which passes to the extensor surface of the leg. This artery passes through the proximal end of the tibiofibular interspace and takes a recurrent course toward the knee. The proximal part of the artery takes part in the formation of the adult a. tibialis anterior. It may be referred to as the ramus perforans cruris. The recurrent vessel continuing from the r. perforans cruris is the arteria recurrens tibialis anterior of the adult.

The points marked upon the axial artery by means of the r. communicans superius and by the origin of the r. perforans cruris, respectively, may be used for the convenient subdivision of the vessel into three parts. The part upon the proximal side of the r. communicans superius will be referred to as the a. ischiadica and that upon the distal side of the r. perforans cruris

r. muse, artic. a. femor. a. epigost inf

r. saphen. I I ^^ a iliaca ext.

r. recur, t. a. I 1 •5;^^wc^c-^ ^ .^^msr aorta. r. pert crur.

r pert, tarsi.

rs.v

rete dorsal.\

rpte plantar I /'

a. interoSf' j \

a popl. prof ja. peron. p superf. a. plant med. (cut)

atib.p. superf.

4

r saphen. rete plantar a popl. prof, a inter OS I

a. qlitaea. a. ischiad.

r muse artic. a.epigast. inf. a iliac ext a iliac com

a. plant, lot. / W peron \ n. obtur a. peron p. superf\ a. tib. p. superf

a. plant, med. a. /sc/i/od.

a. glutaea sup.

F.E.r

,0. tib. p superf. r. saphen r muse artic. a plant med. \a. genu, inf med.l / a circ. fern. /at. a coronar\ \ \ / \ a epigast inf

a iliac, ext.

r com inf. a plant lat i i/calclat

a. popl prof, a peron. '/?. superf. a. ischiad

a glutaea. sup.

rr.P

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). Medial aspect. X 20 diams.

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). Medial aspect. X 20 diams.

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.I.C, 409) X 20 diams.

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70 H. D. SENIOR

as the a. interossea. The intervening part 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 arteries resembles, in a general way, the a. tibialis posterior of the adult, it may be called the a. tibialis posterior superficialis. The other slightly more distal in its place of origin is the a. peronaea posterior superficialis (of Hyrtl),^ 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 Upon the medial 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 medialis. The part of the artery which enters the sole becomes the a. plantaris medialis of the adult.

The a. peronaea posterior superficialis passes from the medial to the lateral aspect of the n. tibialis by skirting around the proximal and lateral sides 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 branch. The branches are both short and end blindly.

Two branches now spring from the lateral side of the a. femoralis. 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 adjective '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.

This is resolved later into the rami musculares for the mm. popliteus, tibialis posterior, flexor digitorum longus, and flexor longus hallucis.

ARTERIES OF HUMAN LOWER EXTREMITY 71

e. Stage of 17.8 mm. H. E. C, no. 839,^ figs. 5 and 9 E

During the preceding stages of development the arterial retia of the foot have received their blood supply 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 superficialis 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. tibialis posterior superficialis and the rete plantare becomes the a. plantaris lateralis of the adult foot. At the present stage of development it receives blood from two sources.

3 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 bj^ Thyng (Am. Jour. Anat., vol. 7, p. 489) and by Thyng and Lewis (Am. Jour. Anat., vol. 7, p. .505) as an embryo of 13.6 mm. The distribution of the arteries of the lower extremity resembles that of other embryos of about 15 or 16 mm.

72 H. D. SENIOR

The part of the a. tibiahs posterior superficiaUs distal to the newly formed origin of the a. plantaris lateralis now becomes the a. plantaris medialis. 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 constituting a (transitory) superficial plantar arch.

The a. tibialis anterior, pars distaUs, 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 tibiahs anterior. The portion which extends from the a. poplitea profunda to the pars distalis enters into the composition of the adult a. tibiahs 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 direct 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 caliber of the a. femoralis has gradually exceeded that of the a. ischiadica, which has now become exceedingly slender. After having traversed the lower portion of the sacropudendal plexus, the a. ischiadica passes.

ARTERIES OF HUMAN LOWER EXTREMITY 73

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

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 be clearly recognized, since it is possible to identify the individual muscles of the limb.

The a. poplitea profunda runs between the m. popliteus and the tibia. 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 superficialis. This short trunk, which lies upon the posterior surface of the m. popliteus, may now be called the a. poplitea superficialis. 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 the 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.

1° In this vessel lies, according to Hyrtl, the key to the deep supramalleolar anastomosis (i.e., the r. communicans) between the a. peronaea 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.

74 H. D. SENIOR

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 posterior 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 unsuitable for reproduction. The data gained from an €xamination of its separate parts are embodied in two diagrams (fig 7, A and B) which may serve as a rough guide to the interpretation 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 malleolus 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 superficialis, 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 com

AETERIES OF HUMAN LOWER EXTREMITY

75

municating branch which foreshadows the development of the future a. peronaea.

. The communicating branch in question leaves the a. peronaea posterior superficialis at the proximal border of the m. flexor hallucis longus. It passes distally between the mm. flexor hallucis longus and tibialis posterior to join the a. interossea,

t.p., m.

d.l.,m.

tp.. m.

hl.m.

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. I. m. flexor digitorum longus; h. I., m. flexor hallucis longus; t. p., m. tibialis posterior.

as that artery lies upon the interosseous membrane. It may be called the r. communicans inferius.

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

76 • H. D, SENIOR

proximal and distal ends of the r. communicans inferior are respectively connected also take part in the formation of the a. peronaea.

Of the branches of the a. femoralis, those arising from the lateral side are identical with the branches of the preceding stage. There are three branches upon the medial side. The 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. I. 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 esmbryonic r. saphenus. The root of the latter branch, therefore, 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 the embryonic 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 which, since it pierces the adductores brevis and magus, represents the first or second of the adult series. The single a. perforans is connected, by means of an extensive plexus, with the more distal section of the now interrupted a. ischiadica.

ARTERIES OF HUMAN LOWER EXTREMITY 77

The a. ischiadica passes through the sacropudendal plexus 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 by 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 surfa.ce of the m. adductor magnus, but has lost its continuity with the a. popUtea. The other vessel participating in the formation 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 been provided by the appearance of a vessel which, passing around the distal border of the m. popliteus, connects the 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 of development involve the vessels which participate in the 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

78

H. D. SENIOR

a. iliolumb.

a. iliaca. com 0. ilioca. exi Q. hypogast a. epigast. inf. a. arc. il. prof, a. pudend. ext a. circ. fern. lat. a. prof, fern or. a. genu, supre r r. muse, et artic

r saphen

a. genu. inf. med.

a. ijb. p. super f.

a. coronar

r. pert (arteriae pero^

rete calc

a. plant med. (cut)

r. profund.

d. perforans. 0. ischiad

a. glutaea sup. sac. lot.

t,lSi — o. glut. inf.

a. genu med.

a pop/ prof.

a. popl. superf.

r conn. med.

a. peron. p. superf.

a peronaea.

a. interos.

a peron. p. superf.

ram. calcan. Iqt. a. plant, lat arcus plant

T.I.V

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.

ARTERIES OF HUMAN LOWER EXTREMITY 79

inferius has practically disappeared. The portion immediately beyond the distal end of the latter vessel Ues 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. poplitea superficialis to the proximal end of the r. communicans inferius persists to become a part of the adult a. peronaea. A large part of the remainder of the artery has been lost, but the distal portion of the vessel can still be recognized as forming a projection upon the proximal aspect of the rete calcaneum. This portion of the artery can be traced through the meshes of the rete as far as the a. plantaris lateralis.

The rete calcaneum is very extensive at this stage of development and occupies the concavity upon the medial side" of the calcaneum and surrounds the deep flexor tendons in 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 superficialis. The part between the aa. flexor hallucis longus and tibialis posterior represents the entire r. communicans inferius. The immediately succeeding part, which rests upon the membrana interossea, is derived from the a. interossea. The terminal part of the artery consists mainly of the r. calcaneus laterahs of the a. peronaea posterior superficialis. 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

THE AMERICAN JOURNAL OF ANATOMY, VOL. 25, NO. 1

aorta. — a mes. inf.

{o. umb'ilic radix ventr radi^ dors a. axis.^ c.pudend.int. plex. pelv.

A 6 mm.

a. circ. il. prof. o. circ. fern, lot Q. prof, femor.

cf. glutaea. sup. a. glut. Inf. a, epigast. inf.

n. cut. fern, post

a. glut. inf. a. perforons. a. genu, suprem. a. pop!, superf. a. t'ib. p. superf. a. peron. p. superf. rete calcan. a. plant, med.

0. peron. p. superf.

a. pcronoea. / a. plont. lot.

Q.Cor^al. ped. Q.zz mm.

9

r.^T'

Fig. 9 Reconstructions showing the arteries of the right lower extremity in the seven human embryos shown in the preceding figures. The 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

o. fervor.

a. ep'igast. inf. r. scphen. n. saphen

f. com. sup. n. obtur. a. axis r. perf. tarsi rete plantar.

n. tibial.

C. II mm.

a. tlloca exT. a epigost inf. a. circ. fern, lot)

a. fern or. a. ischiad. a. Tib. p. superf. a peron. p. superf. a. pop I. prof a. recant, a. r perf crur a. inter OS. r. perf tarsi, rete. plantar.

o. ilioo ext. a. epigost int ore. fern. lot.

a. genu. Inf. med a. recur, t.a. a.tib.ant p.dista/..

\a. pudend inf a. Ischiad.

a. epigast. inf a. circ.fem. ,ht r. muse.-artie., r. saphen.

fib. p. supprf. a. peron. p. s uperf.

r. calc. lot. r. com. inf. a. plant, fat r pprf. tarsi, rete plantar.

a. ischiad. a. popl. prof, a. tib. p-superf a. peron. p. superf. a. plant, med.

plant, lot.

perf. tarsi. rete plantar ir.e mm.

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 portion of the a. peronaea posterior superficialis 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 proximal end upon the posterior surface of its interosseous membrane. This vestigial branch occasionally persists as a branch of the adult a. tibiaUs 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 branches known as the r. calcaneus medialis of the a. plantaris lateralis.

The aa iliolumbaUs and sacralis lateralis now arise from the a. glutaea superior. The root of the latter artery has consequently become the posterior division of the adult a. hypogastrica. All the visceral arteries of the pelvis, with the exception of the a. vesicalis superior, have assumed their adult relations.

h. Changes occurring in the principal arteries subsequent to the 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 development. 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. interosseus 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 popUteal region to reach the r, perforans cruris through the original channel, namely the a. poplitea profunda. The a. poplitea superficialis is longer than at the stage of 18 mm., having increased in length at the expense of the aa. tibialis posterior superficialis 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

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. to., a. genu media; i., a. interossea; i. 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. communicans medius. Blood may now pass from the proximal part of the a. poplitea profunda to the a. tibialis anterior, pars distalis by two routes: 1) anterior to the m. popliteus, by way of the distal part of the a. poplitea profunda and r. perforans cruris, or 2) posterior to the m. popliteus, by way of the a. poplitea superficialis, developing a. peronaea, r. communicans medius, a. poplitea profunda, and r. perforans cruris.

At the stage of 24.5 mm. (fig. 10, C) the direct arterial route upon the anterior surface of the m. popliteus has ceased to exist. The part of the a. pophtea profunda not incorporated in the definitive a. pophtea or tibiahs 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. pophtea 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 distahs.

The a. poplitea superficialis reaches completion at the stage of 24.5 mm. by extending as far as the r. communicans medius which then becomes one of its terminal branches. By this means the a. peronaea rehnquishes its temporary participation in the formation of the a. tibialis anterior.

B. The conversion of the embryonic a. tibialis posterior superficialis into the adult a. tibialis posterior.

The 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 pophteal 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. peronaea from the terroination of the a. pophtea to a point upon the a. tibialis posterior.

After the formation of the a. tibiahs posterior has been completed by the occurrence of these changes the vessel still retains its original relation to the n. tibiahs. The relations between the a. poplitea and the n. tibialis also differ from those of the adult.

The entire a. pophtea hes upon the medial side of the n. tibialis. The a. tibialis posterior crosses the medial side of the nerve to gain its posterior aspect upon which it runs until it ends behind the medial malleolus. The relations of the aa. poplitea and tibialis posterior to the n. tibialis have been thoroughly studied up to the stage of 22 mm. They seem to remain unaltered in the oldest serially cut embryo which has been examined in this regard. It is C. I, E. C, no. 1134, which measures 33.5 mm.

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 w^ould 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. i- The relaMons, 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 wdth 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 to the V. hypogastrica, the otlier to the v. femoralis.

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

12 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. umbiHcaHs, 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 superficialis, 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. tibialis 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 subdivision 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. dorsalis pedis. This artery is a channel through the embryonic rete dorsale. Its importance dates from the appearance of the distal part of the a. tibiahs anterior which is developed between the stages of 15 and 16 mm.

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.

Branches. One of the adult rr. tarseae laterales represents the dorsal end of the r. perforans tarsi, all other branches are derived from the rete dorsale.

A. femoralis. This artery arises from the a. iliaca 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. Although this 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 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 the part of the r. saphenus upon the proximal side of the origin of the rr. musculares and articulares. These branches arise directly from the a. femoralis, but have migrated to the embryonic r. saphenus by the stage of 22 mm. The distal portion of the latter vessel corresponds to the r. saphenus of the adult.

A. hypogastrica. 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 anterior division of the a. hypogastrica is derived from the proximal part of the a. axis, which becomes the a. glutaea inferior, from the root of the a. pudenda interna, and from the part of the a. umbilicaHs beyond the distal end of its dorsal root. The portion of the original a. umbihcalis which contributes to the formation of the a. hypogastrica is the source, in all probability, 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 sacrahs lateralis to the a. glutaea superior, the proximal part of that artery becomes the posterior division of the a. hypogastrica.

A. iliaca communis. This artery is derived from the portion of the dorsal root of the a, umbihcalis which lies upon the proximal side of the origin of the a. iliaca externa.

A. iliaca externa. This artery already springs from the convexity of the a. iliaca 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. circumfiexa ileum profunda arise from the a. ihaca 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. tibiaUs posterior. This artery has given origin to the r. coronarius at the stage of 18 mm. and to the r. perforans and to the 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 inferius disappears between the stages 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).

The branches which arise from this portion of the a. interossea are transferred to the a.' peronaea. They are the r. coronarius malleolaris, part of which becomes the adult 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 axial 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, follows the V. ischiadica and the n. cutaneus femoris to the 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 magnus.

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 a 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 superficialis and of the entire r. calcaneus lateralis of that vessel (p. 74).

Branches. The r. perforans and r. communicans, belong orig'nally to the a. interossea. The rr. calcanei laterales are . branches of the r. calcaneus lateralis of the a. peronaea posterior superficialis.

A. peronaea posterior super ficialis. The course of this embryonic artery is described on pages 70 and 74. The main stein 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. peronaea posterior superficiahs unites with the a. tibialis posterior superficiahs to form the a. pophtea superficiahs and the part of the a. tibiahs 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 branches of the a. peronaea posterior superficiahs 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 laterahs, which arises from the a. peronaea posterior superficiahs 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 lateralis. The proximal part of this artery represents the medial terminal branch of the a. peronaea posterior superficiahs (p. 71), which unites with the a. tibialis posterior superficiahs. The distal part represents the lateral terminal part of the same vessel.

Branches. The r. calcaneus medialis represents the terminal portion of the main trunk of the embrj^onic a. peronaea posterior superficiahs. The arcus plantaris and all its branches are deriA^ed from the embryonic rete plantare.

A. plantaris medialis. This artery is the distal portion of the embryonic a. tibialis posterior superficiahs. It is marked off from the remainder of that vessel by the medial terminal branch of the embryonic a. peronaea posterior superficiahs.

A. poplitea. The part of this artery above the origin of the a. genu inferior medialis represents a surviving portion of the embryonic a. poplitea profunda (p. 73). The part lying upon the posterior surface of that muscle represents the embryonic a. poplitea superficiahs. The proximal portion of the a. genu inferior medialis 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.

A. poplitea profunda. The course of this vessel is described on page 73. The part of the a. poplitea profunda which extends from the hiatus tendineus to the origin of the a. genu inferior medialis becomes the proximal 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 super ficialis. 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).

A. tibialis anterior. This vessel may be divided into four parts which correspond to the four embryonic components of the adult artery.

The first part extends from the origin of the vessel to the root of the a. recurrens tibialis 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 point immediately beyond the root of the a. recurrens tibialis anterior. It is derived from the proximal portion of embryonic r. perforans cruris (p. 68).

The fourth part of the artery extends from the termination of the third part to the proximal end of the a. dorsalis pedis. It represents the entire a. tibialis anterior, pars distalis, of the embryo (p. 72).

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 which 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 adult.

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

Branches. The a. peronaea is described on page 90. The a. malleolaris posterior medialis and the r. communicans are derived from the embryonic r. coronarius malleolaris medialis of the a. interossea (p. 73).

A. tibialis posterior superficialis. 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 superficialis persists in the adult life. In combination with the a. peronaea posterior superficialis, 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. tibiahs posterior beyond the origin of the a. peronaea and as the a. plantaria medialis.

The relation of the part of the a. tibialis posterior superficialis 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.

BIBLIOGRAPHY

Caillard 1832 Proportions de Med. et de la Chir. These inaug., Paris.

Cruveilhier, J. 1843 Traite d'Anotomie descriptive. Paris.

DeVriese, Bertha 1902 Recherches sur revolution des vaisseux sanguins

chez I'homme. Archiv. de Biologie, T. 18, p. 665. Dubrueil, J. M. 1847 Des anomalies arterielles, Paris. Ellis, G. V. 1853 An account of an instance of remarkable deformity of the

lower limbs. Medico-Chir. Trans., vol. 36, p. 439. Fagge, C. H. 1864 Case of aneurism seated on an abnormal main artery of

the lower limb. Guy's Hosp. Rep., vol. 10, p. 15. Froriep, L. Fr. V. 1832. Notizen aus dem Gebiete der Natur u. Heilkunde,

B. 34, S. 45. Green, P. H. 1832 On a new variety of the femoral artery, with observations.

Lancet for 1831, vol. 1, p. 731. Grosser, O. 1901 Zur Anat. u. Entwichlungsges. des Gefass-systems der

Chiropteren. Anat. Hefte, B. 17, H. 2, S. 203. HocHSTETTER, F. 1890 tjber die urspilingliche hauptschlagader der hinteren

Gliedmasse des Menschen, u.s.w. Morph. Jahrb., B. 16, S. 300. Hyrtl, J. 1864 tiber normal u. abnorme Verhaltnisse der Schlagadern des

Unterschenkels. Wien. Leboucq 1893 Verhandl. d. Anatom. Gesellsch., auf. d. siebenten Versamml.

Anat. Anz., Erganzungsh. zum. B. 8. Levy, G. 1902 Morphologia delle arteriae iliache. Parte 2. Archiv. Ital. di

Anat. e di Embriol., V. 295. McMuRRiCH, J. P. 1904 The development of the human body, 2nd ed., Philadelphia. PoPOWSKi, J. 1893 ijberbleibsel der Arteria saphena beim Menschen. Anat.

Anz., B. 8, S. 580.

1894 Das Arteriensystem der unteren Extremitaten bei den Primaten.

Anat. Anz., B. 10, S. 55 u. 99. Qtjain, R. 1844 The anatomy of the arteries of the human body. London. RxJG, C. 1863 Anomalie der Arteria cruralis. Wtirzb. mediz. Zeits., B. 4,

S. 344. RuGE, G. 1894 Varietaten im Gebiete der Arteria femoralis des Menschen.

Morph. Jahrb., B. 22, S. 161. Salvi 1898 Arteria dorsalis pedis. Pisa. Senior, H. D. 1917 The development of the external iliac artery in man.

Ann. N. Y. Acad. Sci., vol. 27. Stieda, H. 1893 Verhandl d. Anatom. Gesellsch., auf d. siebenten VersammL

Anat., Anz.. Erganzungsh. zum B. 8.

SuESSDORF, M. 1895 Lehrbuch der vergleichenden Anatomie der Haustiere.

Stuttgart. Tandler, J. 1903 Zur Entwickelungsges. der menschlichen Darmarterien.

Anat. Hefte, B. 23, H. 1, S. 187. Velpeau 1839 Elements de Medicine Operatoire. Zagorski 1809 Mem. de I'Academ. des Sci. de Petersb. Zuckerkandl 1894 Zur Anat. u. Entwickelungsges. der Arterien des Vor derarms (1. theil). Anat. Hefte, B. 4, H. 1, S. 1.

1895 Zur Anat. u. Entwickelungsges. der Arterien des Unterschenkels

u. des Fusses. Anat. Hefte, B. 5, H. 2, S. 207.