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

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

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

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

XVIII. Development of Blood, Vascular System and Spleen: Introduction | Origin of the Angioblast and Development of the Blood | Development of the Heart | The Development of the Vascular System | General | Special Development of the Blood-vessels | Origin of the Blood-vascular System | Blood-vascular System in Series of Human Embryos | Arteries | Veins | Development of the Lymphatic System | Development of the Spleen
Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

A. Origin of the Vascular System.


The question of the source of the cells which form the vascular system still remains, as it has for a long time, one of the most disputed problems of mammalian and indeed of general vertebrate embryology. The question has met no undisputed solution for the case of any vertebrate, and here, in contrast to the dearth of human material, we can possess a wealth of all the necessary stages. When such fundamental questions as the genetic relation between extra-embryonic and embryonic vessels, and indeed even the method of origin of the former — the well-known vitelline vascular anlagen — are still unsettled, and when we consider the paucity of these earlier stages which should be necessary for the determination of this question in man, a speedy solution of the problem in human ontogeny is expected by no one.


u Such, for instance, as that of the upper thoracic aorta on the columna vertebralis. Whereas in enibryos of 20 mm. the upper aa. intercostales find their interstitia intercostalia at the same level, in the adult, as is well known, they must course upwards to reach their interspaces.


13 When completing the present account of the development of the human vascular system, I had access to six young embryos in the possession of Professors Kollman, Eternod, R. Meyer, Strahl and Felix. These were studied in the laboratory of Professor Wiedersheim in Freiburg i. B. To all of these gentlemen I wish to express my sincere thanks. Four very valuable ernbryos in the collection of Graf Spee were studied in his institute in Kiel, for which great privilege I am deeply indebted.


If, then, we posses no safe generalizations with which to interpret the few observations possible on human embryos, we are also still further retarded by certain peculiarities of the early history of the primate embryo which affect profoundly the vascular system. The presence of an early vascularized belly stalk and chorion distorts the entire sequence of tbe usual development of the vessels and furnishes us at once in embryos astonishingly young with highly specialized and characteristic phenomena. These latter facts are now beyond doubt and I shall present them briefly below. Here only it need be remarked that the early history of the human vascular sj-stem has not enabled us as yet to make any statement as to the exact cellular origin of the endothelium in man. The only facts in the human embryo's history which may be brought into relation with this important question seem to point clearly to a mesodermal source for the primary blood-vessels. These are: 1. The abundant vascularization of the early chorion, where apparently any role of the entoderm can be excluded. 14 2. The early vitelline vascular anlagen which cause a characteristic " hummocking " of the yolk-sac wall lie in the mesodermal coat of the latter and are sharply separated from the entoderm.


3. The earliest vascular cells within the body of the embryo (in the Graf Spee embryo " Glaevecke " ) are certainly in more intimate relation with the mesodermal than with the entodermal cell layer.


B. Description of the Vascular System Present in Early Human Embryos.


EMBKYOS WHICH AS YET POSSESS XO MESODEKMIC SOMITES.


It is certain that long before any vessels are present in the body of the human embryo, and at a time so early as considerably to precede the formation of any somites, typical " vascular anlagen" are found scattered over the ventral pole of the yolk-sac.


In those mammals which, like the rabbit, possess a vitelline vascular area of the limited circular form, bounded by a marginal sinus, which characterizes the lower vertebrates, it is probable that the vascular anlagen first form in a ring-like row around the borders of the future area vasculosa, as Van der Stricht has described for the rabbit. But in the primates (and presumably in all other mammals in which the yolk suffers a complete overgrowth by the area vasculosa, — e.g., carnivores and artiodactyls) the vascular anlagen are most irregularly scattered, covering at an early date the whole ventral surface and soon all the yolk-sac.


These vascular anlagen or blood islands, as in other vertebrates, appear as nodular swellings of the wall of the yolk-sac, and consist microscopically of circumscribed cell clumps lying between the mesoderm and entoderm. The cells of these clumps very early show a differentiation into centrally lying blood-cells and a row of peripheral bounding cells, — the endothelium. The best-developed, and hence earliest, of these anlagen are situated more ventrally, the younger nearer the body of the embryo, in very early stages they can be shown to be concerned in the formation of the vessels in the belly stalk (aa. umbilicales), and these vessels belonging to the placental circulation, are so exaggerated in development as to precede the appearance of vessels in the embryonic body proper. Furthermore, as Eternod discovered, when, later, the vascular trunks of the embryo proper make their appearance (the aorta? and vv. umbilicales), they are already connected with the chorionic capillaries through the precocious aa. umbilicales


  • It may perhaps be mentioned that those who, like Hubrecht (190S), consider that a considerable part of the early mesoblast has really come from the entoderm will dispute the above statement.



Fig. 401. — Section of a vascular anlage in the wall of the yolk-sac in the human embryo 2 mm. long shown in Fig. 408. E., entoderm; V., vascular cells; M., usual mesoderm cells.



M.


Fig. 402. — Section of a more advanced vascular anlage from the yolk-sac of the same embryo as shown in Fig. 401. EC endothelial cell.


Fig. 403. — Section of a well-developed vessel from the same yolk-sac.


and w. chorioplacentares, and so it comes about in the human embryo that an umbilical circulation exists in embryos so young that the mesoderm is as yet unsegniented into somites.


The embryos which I have been able to examine with respect to their early vessels constitute, together with that so fully described by Eternod, the following series, given in order of their probable age.



Designation of embryo.



Length of embryonic shield .



Collection.



Literature.



Von H(erff) . .37 mm. Graf Spee Graf Spee, Arch. f. Anat. u. Phy., 1896.


Frassi, NT. 1 1 . 17 mm. Prof. Keibel Frassi, Arch, f . mik. Anat., Bd. 70 u. 71.


Glaevecke. . . 1 . 54 mm. Graf Spee Graf Spee, Arch. Anat. u. Phy., 1S89, 1896.


Eternod 1.3 mm. Prof. Eternod Eternod, Anat. Anz., Bd. xv, No. 11, 12, 1898.



For further descriptions of the embryos themselves the reader is referred to Chapter TV of the present work, where this has been done by Prof. Keibel. Here we need be concerned only with remarks on what blood-vessels are present.


The embryo von Herff, the youngest, and probably only consisting of the region of the primitive streak, possesses abundant vascular anlagen scattered over the entire ventral and part of the. lateral surfaces of the yolk-sac, reaching often to the angle of junction of the yolk-sac with the embryonic shield. Whereas in general those of the anlagen whose development seems most advanced are more ventrally situated, there exist also many not widely separated from the embryonic body, in which an evident differentiation into endothelium and blood-cells has come about. In the belly stalk and chorion of this embryo there are, as Graf Spee has described, highly characteristic strands of spindle cells, which often consist of a double row of nuclei and, again, may enclose a distinct lumen. These cells appear to keep to themselves, and to constitute a single unified but widely branched tissue which grows oftenest in strands frequently anastomosing among themselves. This tendency to constitute a distinct tissue element different from the connective tissue, together with the histological appearance of longer oval nuclei and more deeply staining cytoplasm, suggests strongly that we may be dealing here with endothelium, a conviction strengthened by the typical vascular appearance given in those instances where the cells surround a distinct lumen. 15 The embryo Frassi, which now, besides the primitive streak region, shows a considerable embryonic area in front of this (the two being separated by a typical canalis neurentericus) also exhibits many evident blood-vessels. Not only have we here again an abundance of well-differentiated vascular anlagen on the ventral walls of the yolk-sac, but in many of the sections through the belly stalk vessels can be recognized (one of these being especially large), and this is also the case in the chorion.


The embryo Glaevecke of Graf Spee (NT. 2) contains, besides many yolk vascular anlagen and chorionic vessels seen in the preceding stage, the first vascular cells within the body of the embryo itself. In the region of the heart these constitute a true typical endothelial anlage for that organ (Fig 404), but also further caudalward there can be recognized many cell strands clearly isolated and different in character from the endoderm and mesoderm between which they lie; they thus occupy the typical position for, and present the typical appearance of, early vascular cells 16 (Fig. 405). At first lying about half-way between the point of insertion of the yolk-sac and the mid-line of the body, they gradually shift lateralward, and before the neurenteric canal is reached occur quite exclusively only at the 15 If such an interpretation be correct we must have a remarkable growth of the endothelium in the chorionic membrane of young human embryos, for there occurs here no coincident development of blood-cells, as is typically the case in the vitelline anlagen. These cells of the chorion (Spee's so-called spindle-cells) are present in relatively great numbers and, so far as I am aware, cannot be distinguished from similar cells in still younger embryos (e.g., that recently demonstrated by Fetzer [1910] ), where we are quite unable to distinguish vascular beginnings on the yolk-sac proper. The above suggestion, however, appears to me forced on one who now takes up the study of a series of progressively slightly older stages, such as we have in the embryos here dealt with, where difficulty would be experienced in separating these cells from those which gradually are concerned in the formation of undoubted vessels.


16 Concerning the origin of these intra-embryonic vascular cells, it can only be said that the histological appearances are inconclusive, and one may often see what might be taken for a genetic connection of the cells with the intermediate mass of the mesoderm as Mollier (1906) has reported in reptilian and avian embryos. On the other hand, however, the series of sections does not permit one to exclude the strong possibility that these cells constitute a connected unit which could have invaded the embryonic body from the splanchhopleure of the yolk-sac.


lateral margins of the embryonic area and very near the insertion of the yolk-sac. In the area behind the neurenteric canal these cells apparently retreat to the upper margin of the yolk-sac proper. This parallels the condition found in this area in the younger embryo von Herff. Finally, as the allantois is given off, these vascular anlagen can be traced into vessels which in the belly stalk lie at first on either side of and soon below the allantoic diverticulum; they are consequently in the position typical for the umbilical arteries and doubtless represent the anlagen of these vessels in the belly stalk.


We turn now to the embryo described by Eternod (1898) and in which we have the earliest circulatory conditions in the human embryo. However, a considerable gap exists between the stages which we have just been considering and that depicted by Eternod, for in the latter case a system of vessels are now present coursing through the body of the embryo, — the aorta? and umbilical veins. Exactly how these first vessels are formed in man is as yet unknown. The umbilical veins, the heart, the aorta? and umbilical arteries, and, finally, the chorionic capillaries, form the simple vascular cycle here present (Fig. 406)." The Eternod embryo measures approximately 1.3 millimetres in length and has also as yet no indication of mesodermic somites. It shows an anteriorly placed heart, the short aortic end of which, doubtless representing the future bulbus aortae aud aorta ventralis, gives off the aortic arch 18 which sweeps up on each side to the primitive aorta. The aortas course dorsal to the head-gut and on either side of the notochordal plate, and at last turning down sharply into the belly





Fig. 404. — Cross section of the human embryo Glaevecke (collection of Graf Spee), taken just in front of the anterior intestinal portal, showing the vascular cells constituting the anlage of the endothelium of the heart. X 113.


17 As yet, though there are many vessels on the yolk-sac, particularly on its ventral surface, no evidence for a vitelline circulation exists, for no connections between these capillaries and the aorta? can be traced. This, the most revolutionary result of Eternod's study, appears to place man unique among mammals in the ontogenetic precedence of the umbilical over the vitelline circulation, for in the mammalia generally, as is well known, the yolk-sac circulation is always primary.



Vessel-forming cells


Vessel-forming cells

Vessel-forming cells

Vessel-forming cells


Vessel-forming cells Vessel-forming cells


yolk-sac vessels

Anlage of yolk-sac vessels


Anlage of the aa. umbilicales


Anlage of the aa. umbilicales

Fig. 405. — A series of sections through the human embryo Glaevecke, showing the earliest intra-embryonal vascular cells and the anlage of the aa. umbilicales in the oelly stalk.


stalk, run out onto the chorion without having given any branches into the tissues of the embryo. The umbilical veins (w. umbilicales primitives), which collect the blood from the extensive chorionic vessels (w. chorio-placentares), unite in i lie belly stalk into a single trunk (v. umbilicalis Lmpar) 3 but again pari as the embryo proper is reached, and course in the body wall on either side near the attachment of the amnion. Just as they begin their embryonic course, each umbilical vein receives a large tributary from the capillary plexus nf the yolk-sac, and these two tributaries anastomose with one another on the wall of the yolk-sac so that a venous ring is produced enclosing the allantois (ansa vitellina). The significance of this is unknown. This connection of the vitelline vessels with the umbilical vein gives the possibility of an early drainage of the yolk-sac in that direction were any aortic afferents traceable to the vitelline plexus. But at a time when such afferents clearly supply the vitelline plexus, the true vitelline veins are formed, so that at the time when we are first able to affirm the possibility of a complete vitelline circulation it is supplied and drained, as in all mammals, by its own system of vessels.


M It is certain that we are not dealing here with three aortic arches and that the picture given by Eternod is somewhat schematized, the small irregular vessels here likely being persisting strands of a capillary plexus. (See Fig. 398 of a duck.)



Fig. 400. — Lateral view of the vascular sj stem in a human embryo 1.3 mm. long, without somites. (After Eternod, from Kollmann, Handatlas der Entw. d. Mensehen. 1S97 ' »g. 512.)


18 EMBEYOS POSSESSING FKOM SIX TO EIGHT SOMITES.


Unfortunately, we possess as yet no human embryos belonging to the interesting period in which the first five somites are formed, but for stages only shortly after this several excellently preserved and trustworthy specimens are now known. I base what can be said about the vascular system at this stage chiefly on the study of the following four embryos : 20

Designation of embryo.


Number of somites.


Collection.


Literature.


PfannenstielKroemer NT. 3 5-6 somites • •


[Keibel-Elze, 1908.




[Felix, 1910.


Graf Spee embryo ....


Mall No. 391 .


6-7 somites 7-8 somites


Graf Spee Prof. Mall [Graf Spee, 1887.


Kollmann, 1889, 1907 (Figs. 187 1 and 188). Dandy, 1910.


Eternod's embryo ....


8 somites (the 8th not com





pletely separated) Prof.


A. C. F. Eternod fEternod, 1896, 1899, 1904, 1909. {Kollmann, 1907 (Figs. 183 and 184)

The most striking change which has occurred in the vascular system of these embryos is found in their possession of the first branches of the aorta. The majority of these aortic branches go to the yolk-sac (aa. vitelline primitivae), and, though at present appealing as almost frank lateral branches (Figs. 407 and 444), in later stages are shifted so as to come off more ventrally.


The primitive vitelline arteries form an irregular series of connections between the aortse and the vitelline capillary plexus which has arisen out of the early yolk anlagen. They are not, as

19 Eternod has pointed out that in the Selenka specimen of Hylobates the vitelline plexus is also shown in connection with the chorionic vessels by means of two stems which surround the allantoic tube in reaching the belly stalk, and in the latter they fuse to a single large vessel (v. umbilicus impar) which can be traced into the chorionic vascular tree. The ansa vitellina may consequently be a characteristic primate structure, but it is impossible in the light of present knowledge to assign to it any significance. It is quite possible that these vessels merely represent a persisting connection of the vitelline and chorionic vessels indicating a primitive common anlage.


The manuscripts of Dandy and of Felix were generously placed at my disposal by their authors and were of much service during the study of the embryos concerned.


a rule, at first segmentally arranged. Cephalad they may extend as far as the first intersegmental cleft, as Dandy (1910) first showed. In the Pfannensteil-Kroemer embryo the first of these appear opposite the third somite on the left, and in the Eternod embryo between the third and fourth somite on the right. Occurring generally so frequently as to be opposite each somite thereafter (though they occupy no constant position with regard to the somite mass), when the unsegmented mesoderm is reached they are found in far greater numbers, and eventually resolve the termination of the aorta itself into a plexus of capillary-like vessels not unlike that to be seen in injections of chick embryos. 21 With


Fig. 407. — Cross section of a human embryo with six somites (NT. 3), in the region caudal to the last somite, showing the delicate aorta and their vitelline branches.



this plexus, as Felix (1910) has shown, and as I can confirm, the umbilical artery is in connection and so by these multiple roots takes its origin from the aorta. It is by means also of the farther caudal growth of this plexus that the aorta is continued caudally and the a. umbilicalis wanders caudalward through a considerable distance. These facts establish clearly that the umbilical artery is

21 Felix (1910) is unable to follow the aorta throughout its entire extent in the first of the above embryos (NT. 3). indicating his belief that it is not present in some places (see his account, p. 603). I am not able to agree #with his account, nor with his statement concerning the intestinal vessels (p. 606) — " cranialwarts offnen sich seine Gefasse teilweise frei in die primare Leibeshohle " !

596 merely a modified vitelline vessel; for a considerable time its roots of origin from the aorta are indistiguishable from the row of primary vitelline arteries.


Headward the vitelline plexus is connected on each side with the heart by two primitive vitelline veins, which receive the umbilical veins which have coursed in the somatopleure and then turn in sharply from their lateral position to gain the heart; in doing



Fig. 408. — Dorsa view of model of human embryo possessing 7-8 somites, being the same embryo shown in Fig. 23 B (ante, p. 32). Portion of ectoderm of right neural plate is removed, showing thickness of wall and its relation to deeper structures. The three primary cerebral vesicles are indicated. (After Dandy.) All., allantois; Ch.. chorda; Coe., ccelom; Fg., fore-gut; Hg., hind-gut; Ht., heart; Mes., mesoderm; P.c, pericardial ccelom; U ., umbilical arterial sinus; V ., umbilical vein. (Mall, No. 391 J

this they traverse the bar of mesoderm which intervenes between the pericardial cavity and the yolk-sac wall and which is destined to constitute the septum transversum of His. Their course here hence resembles entirely that taken by the terminal portions of the primitive vitelline veins in other very early mammalian embryos {e.g., the rabbit), and 1 present here in lieu of a more detailed description a series of accurate tracings of their course (Fig. 409). Besides the vitelline circulation, which is thus well established



Fig. 409. — A series of sections through the human embryo with 7—8 somites (shown in Fig. 408), showing the relation of the chief venous stems to the heart.



in these embryos, other vascular channels are beginning to be formed; these constitute the first endothelial sprouts to be sent out into the tissues of the embryo proper; arising dorsally from the aorta, they lay the anlage for the a. en rot is interna in the region of the fore- and mid-brain, whereas farther caudally they form a series of presegmental and segmental dorsal offshoots of the aorta. In all cases these tiny vessels are directed to the sides of the neural tube, which consequently, neglecting the primitive gut and yolk-sac, must be considered the first embryonic tissue to receive vessels; this occurs, in fact, before the nervous system is in the form of a tube, for it is, in the first of these embryos, a widely open furrow. Each vessel, having reached the side of the medul


Aorta dorsalis

A part of the plexus vitellinus

a. umbilicalis

Fig/]410. — Reconstruction of the arterial system of a human embryo with 6 somites (NT. 3), seen from the left. (Modified after W. Felix, 1910.)

lary furrow, divides T-like and can be traced a short distance caudally and cephalically. It is by the anastomosis of these branches that in older embryos (those of 15 somites) a longitudinal vessel is established at the sides of the hind-brain and the neural tube caudal to it {v. capitis medialis). The dorsal segmental arteries have long been known, for they occupy accurately the interspaces between the somite masses ; some four of them are already present in the Eternod embryo with 8 somites, and, since these are progressively smaller in size cephalo-caudally, their outgrowth from the aorta quite certainly proceeds in this sequence.


EMBBYOS POSSESSING FBOM THIRTEEN TO FIFTEEN SOMITES.



Designation of embryo.


Number of somites.


Collection.


Literature.


Bulle, NT. 5 Pfannenstiel III, NT. 6 Graf Spee No. 52 13-14 somites 14 somites 15 somites Prof. Kollmann Graf Spee


Kollmann, 1889, 1907. KeibelandElze, 1908 Low, Jour. Anat. and Phys., 1908. Felix, 1910.






__ .



In human embryos which possess some fifteen somites we not only have an increased number of dorsal segmental arteries (eleven

Cauda) most part of otic thickening

v. card. ant.



v. card. ant.



v. vitello umbilicalis communis

v. vitello umbilicalis communis

v. card. ant.



v. vitello; umbilicalis communis d. v. card, ant,

Fig. 411. — A series of cross sections through a human embryo with 15 somites (collection of Graf Spee, No. 52), showing the course and relations of the primitive head vein (v. capitis medialis et v. cardinalis anterior) and the relation of the chief venous stems to the heart.


in the embryo with fifteen somites) and of the primitive vitelline arteries, but also another set of aortic branches which I shall designate as the primitive lateral branches of the aorta. 22 These 22 Graf e (1905) was, I believe, the first to see these vessels, describing them in the posterior portion of a chick embryo of about sixty hours; but their cephalic extension was shown by Williams (1910), who described them in the first two intersegmental clefts.



600 vessels take origin from the lateral aortic wall, often from its ventro-lateral angle, and course obliquely upward and outward in the space between the somite and the intermediate mesodermic mass; here I have seen them anastomose with the cardinal vein; they are also often connected with the dorsal segmental arteries by direct cross anastomoses in the loose mesoderm of the intersomitic clefts.



a. umbilicalis


Aorta dorsalis

Fig. 412. — Reconstruction of the arterial system of a human embryo with 14 somites (NT. 6), seen from the left. (Slightly modified, after W. Felix, 1910.) The primitive vitelline arteries in the area opposite the first five somites have atrophied, but the series of these vessels begins from here caudally to form a continuous row unrelated apparently to metamerism and finally, in the unsegmented area, giving way, as in the younger embryos, to a plexus from which the umbilical artery takes origin.


The first venous channels of the embryo proper — the w. cardinales anteriores — are found at this stage, and in the Graf

DEVELOPMENT OF THE VASCULAR SYSTEM. 601 von Spee embryo with 15 somites can be traced clearly from the region of the optic vesicles, cephalically, to their opening into the common vitelline and umbilical vein, caudal ly. These veins, as Grosser (1907) has shown to be probable for all vertebrates, in man also possess two different and distinct topographical relations, for in their cephalic course they lie close to the sides of the neural tube, constituting the v. capitis medialis, whereas more caudally — i.e., in the region beginning with the first mesodermic somite — they take up a lateral position between the somite and the ccelomic mesoderm where thev may be designated the true vv. eardinales

Right horn of the sinus venosus

Ventral wall of the yolk-sac'


Pericardial cavity Cut edge of the septum transversum

Fig. 413.— Sinus venosus and septum transversum in a human embryo with 14 somites (NT. 6), viewed from above. The right half of the septum has been removed to show the sinus venosus contained therein. (Drawn from the model by Dr. Alex. Low.) anteriores. Opposite the third somite the vessel finally joins the common vitello-umbilical vein by coursing dorsal to the ccelomic cavity in this region (Fig. 411). The v. capitis medialis receives several (four) direct dorsal offshoots from the aorta, so that it really appears as a longitudinal neural anastomosis of these presegmental dorsal arteries ; it turns out rather sharply somewhat in front of the first somite to constitute the true anterior cardinal, which is again formed apparently by a laterally-situated longitudinal anastomosis of loops formed by the dorsal segmental vessels; to it also the primitive lateral branches of the aorta are joined. 23 23 This history of the formation of the anterior cardinal vein in man is thus identical with that which has been previously found in the chick (Evans, 1909), in which latter embryo Williams has recently described the same phenomena in a careful account of the region about the second somite. It is consequently probably significant that the picture furnished by the endothelial cells constituting the first dorsal segmental vessel in the Eternod embryo shows a marked lateral wandering of the endothelium (Fig. 439). This probably should be accounted the first staee in the formation of the anterior cardinal in man.



602 The vitelline veins still behave in all essentials as in the younger stages ; they receive the umbilical veins when quite lateral in position, and the common veins receive the anterior cardinals, turning in sharply to constitute the sinus reuniens (Fig. 411).



EMBKYO OF TWENTY-THEEE SOMITES.



In stages which are intermediate between those which have just been described and embryos possessing limb buds, the posterior cardinal veins develop. This has already occurred in the embryo with twenty-three somites (Eobert Meyer, 300, N.T. 7),


Anastomosis extending along the neural tube

a. umbilicalis

Region of the'om phalomesenteric artery

Fig. 414. — Reconstruction of the arterial system of a human embryo with 23 somites (NT. 7). (Aftei W. Felix, 1910.) *which has no indication as yet of limbs. It is probable that lateral loops of the dorsal segmental arteries are instrumental in the formaton of these veins, as is the case with the anterior cardinals. 24 At this stage the dorsal segmental vessels form in the

24 This method of formation of the posterior cardinal veins appears fundamental. Raffaele (1892) and Hoffman (1893) described it for selachian embryos and Grafe (1905) and the writer have indicated it in the case of the chick.


tissue of the intersomitic clefts large well-marked vascular arches or loops, one limb of which is against the neural tube while the other joins the cardinal vein (Fig. 436). At this stage also the primitive lateral branches of the aorta form an extensive system, and at many levels we are able to find all three systems of branches occurring together and segmentally arranged.


The row of vitelline arteries is by no means exclusively segmentally arranged; nevertheless there is a symmetrical disposition in that these vessels occur in pairs, ^o that in the region in

9th somite



V. cardinalis post.



V. urnbilicalis






X " —v

i .""i^ 3r*wf'f5 I

4 c

J

I* " V - • c » '.a -"'V 1 !

'Aorts

^



V. um "bilicalis

.-'

v (.






i V. omphalomesenterica

  • -^.>

Fig. 415. — Cross section of the human embryo with 23 somites, shown in Fig. 414, taken through the region of the 9th somite, showing paired aa. vitelline.



which the two aortae primitive have fused to a single median aorta we can observe that two vessels arise from the ventral surface of the aorta and course each on its corresponding side of the gut, which possesses as yet no mesentery (Fig. 415). When later an intestinal mesentery is formed, these vessels course for a time side by side, but eventually are completely fused to a medial ventral trunk, or it is possible that one member of the pair gains the ascendency and its fellow atrophies.



604 HUMAN EMBRYOLOGY.


In the posterior region of the body we find not only the posterior cardinal vein, but a new one, lying ventral to the former and near the ccelomic epithelium. This vein, the v. subcardinalis (F. T. Lewis, 1902), has probably arisen by sprouts from the posterior cardinal trunk, as Graefe has shown for the chick; at any rate the presence of a large number of anastomoses between these two vessels speaks strongly for this view. In the region of the mesonephros the subcardinal vein occupies a characteristic position ventral to the )Yolffian duct, but at levels above this region, where we have as yet, according to the view of Felix, only the pronephric anlage, the vein is also found, and in the same position, i.e., ventral to the chief duct, as Fig. 416 will show. There also

12th somite V. card. post.


Principal duct Pronephros Chamber

V. subcardinalis $-fc

Epithelium of the coelom


Fig. 416. — Section showing the position of the v. cardinalis posterior and the v. subcardinalis in a human embryo with 23 somites (NT. 7), taken in the region of the 12th somite.


occurs in embryos of this age another vein medial to the pronephros, and it has probably arisen as a longitudinal anastomosis binding together vascular offshoots from the posterior cardinal veins and also the primitive lateral branches of the aorta. 25 EMBRYO OF 4.9 MM. LENGTH (35 SOMITES, N.T. 14).


By the time the embryo reaches a length of 5 millimetres several important changes in the vascular system have occurred. The embryo described by Ingalls (1907) and shown in Figs. 417, 418 will serve to illustrate this stage.


It will be noted that four complete aortic arches are present, and that another pair — the sixth or pulmonary arches — are being 25 One finds in this embryo pictures which very much resemble that given by Grafe in his table 11, Fig. 7, for a chick of 71 hours.



DEVELOPMENT OF THE VASCULAR SYSTEM. 605 formed by both ventral and dorsal endothelial sprouts. The third pair, the carotid arches, are by far the largest of the series, while the first are already very much reduced. The aortic root on each side now appears to continue toward the head beyond the location of the first arches. This, the internal carotid artery, is doubtless the trunk representing the very early capillary sprouts which the first arch sent toward the brain. It courses headward lateral to the hypophysis and bending dorsally anastomoses with a long branch — the a. vertebralis cerebralis — given off from the first of* the dorsal segmental arteries here present (in this case the hypoglossus artery). At the optic cup the internal carotid gives off the a. ophthalmica as its first branch, and somewhat beyond this a very large branch (a. cerebri ant. et med.) which courses forward between eye and brain; other smaller branches are given off to the mid-brain region, and the carotids then sweep backward to join the cerebral vertebrals, which they furnish with their main volume of blood, although later the stem of origin of the latter vessel gives it most of its blood. The first cervical dorsal segmental artery 26 anastomoses with the hypoglossus, and consequently the path is already furnished for this stem to take over the cerebral vertebral when the hypoglossus yields the current and atrophies. Excluding the hypoglossus vessel twenty-seven dorsal segmental branches arise in pairs from the aorta and sacralis media artery, — i.e., the full number of cervical, thoracic, and lumbar vessels and the first two sacral segmentals. The umbilical arteries, though they later shift to the last lumbar level, arise here opposite the third lumbar segmentals, the remaining lumbar arteries at this stage consequently arising from the a. sacralis media. The aa. umbilicales course medial to the Wolffian ducts, but at the prominent bend which they make in turning upward are in connection with capillaries lying lateral to the Wolffian duct, which ultimately gain a connection with the aortic wall and completely displace the medial roots of origin of these arteries. The subclavian artery arises from the seventh dorsal segmental pair.


Most interesting are the ventral branches of the aorta, for these no longer form a uniform row of vessels, but reflect a beginning differentiation of the gut. Consequently there are retained, besides many smaller ones, three chief branches, to correspond to the stomach-pancreas region, the vitelline-duct region, and the colon respectively (a. cceliaca, a. omplialomesent., et a. mesent. inf.). The middle of these three stems, which is also by far the largest, since it drains yolk-sac as well as gut, takes origin from 20 1 refer to the segmental artery cranial to Hochstetter's "first cervical artery," naming that artery the first cervical which courses with the first cervical nei've, as do Mall. Tandler, and Broman.



Fig. 417. — Reconstruction of the arterial system in a human embryo 4.9 mm. long, lateral view. After Ingalls, Arch. f. mik. Anat., Bd. 70, p. 530, 1907.) A.c, a. cceliaca; A.c. a., a. cerebralis ant.; A.c.s., a. caudalis sin.; Ag., optic vesicle; Al., allantois; A.m.i., a. mes.inf.; A. o., a. ophthalmica; A. omphal., a. omphalomesenterica (with three roots); A. p., a. pulmonalis; A.s., a. subclavia; A.u.s., a. umb. sin.; A. v., a.vertebralis; B. 1,2,8,4,6, aortic arches; C.a.l, first cervical artery; Cd., caudal intestine; D.p., dorsal pancreas; D.i., ductus vitello-intestinalis; Gb., gall-bladder; Ha. , hypoglossus artery; lb., inselbildung; La., lunganlage; M., stomach; Oes., oesophagus; T. a., truncus arteriosus; UK., lower jaw; V., questionable union between the a. vertebralis and a. car. int. (N. T. 14. ) the aorta by four distinct roots. It will be noticed that all these branches are much above their location in the adult, as can be seen by comparing them with the dorsal segmentals opposite, and it is not indeed until the embryo attains a length of from 16 to 20 millimetres that their definitive position is reached.



Fig. 418. — Reconstruction of the venous system of the embryo shown in Fig. 417. A., fibres of the accessorius; C.l, first cervical segment; D.C.8., ductus Cuvieri sin.; F., facialis; G., glossopharyngeus; L.l, first lumbar segment; 0., ear vesicle; 0.1, first occipital segment; S-l, first sacral segment; T., trigeminus; T.l, first thoracic segment; V., union of the left umbilical vein with the liver circulation; V.c.a., v. card, ant.; V.c. p., v. card, post.; V. i., v. ischiadica; V.u.s., v. umb. sin.; V.u. 8.*, remains of the original circulation to the sinus venosus; X., linguo-facial vein.



Irregularly arising, lateral branches of the aorta go to the mesonephros.


In contrast to the earliest stages, the venous system of the embryo proper is now well developed, and one sees the well known fundamental pattern of the two cardinal veins on each side uniting to form the ductus Cuvieri which then joins the umbilical. The anterior cardinal can be seen beginning in two strong efferents in the head region, the first of which doubtless represents the ophthalmic vein. Passing medial to the ganglion of the fifth nerve, the main vein next receives a tributary from the hypophysis region, and continues caudally on the lateral side of the acusticofacial ganglion, the auditory vesicle, and the ganglion of the glossopharyngeus, but medial to the vagus ganglion ; just before reaching the latter nerve, it receives a prominent tributary from the dorsal region (v. cerebri post.. Mall), although smaller tributaries have joined it all along its previous course. Before joining the ductus Cuvieri, several venules run into it, which, from their position and correspondence with the veins of other mammalian embryos, can be recognized as the segmental veins belonging to the first cervical and the several occipital segments. The ductus Cuvieri receives on each side a slender venule, which drains the capillary plexus in the first visceral arch. This vessel crosses from the latter • into the ventral body wall (here constituted by the membrana reuniens over the front of the heart) and runs in this to open into the ductus (v. linguo- facialis, F. T. Lewis, 1909).


The posterior cardinal vein begins at about the level of the third lumbar segment, and courses in the tissue dorsolateral to the Wolffian body. It receives the dorsal segmental veins, which do not become appreciable structures until about the level of the fifth thoracic segment. The seventh cervical segmental vein receives the vessel from the arm bud (the subclavian vein), although this afterward shifts up to the anterior cardinal vein. The v. subcard inalis can first be recognized at about the level of the seventh thoracic somite, and empties into the posterior cardinals at the level of the sixth cervical one. They drain the Wolffian body at this stage, but later acquire greater significance inasmuch as they are incorporated in the formation of the inferior vena cava. The umbilical veins are already sending their main mass of blood into the liver, but with their old connections with the sinus venosus still evident. This uppermost and superficially lying part of the umbilical vein receives tributaries from the arm buds, and this source of blood delays their atrophy (Evans, 1909). The vessels from the lateral body wall also drain into the v. umbilicalis along all of its course until the liver is reached, so that the vein forms at this time an important drainage channel for the entire lateral body wall. The vitelline veins empty their blood directly into the liver sinusoids, the blood from the left omphalomesenteric vein being collected by a short trunk which enters the left horn of the sinus venosus (r. hep. sinistra) ; but the right and larger one possesses a wide passage through this organ to the right horn of the sinus venosus. The two vitelline veins are anastomosed on the ventral, then on the dorsal, and again on the ventral sides of the duodenum, forming thus two venous rings around the gut (His).


EMBRYO OF 7 MM. LENGTH (40 SOMITES, X.T. 28).


The vascular system present in an embryo measuring 7 millimetres begins to be complex enough to demand detailed descriptions for many areas, so that with a brief presentation of the chief features here, we may leave this account of the early vascular system as a whole and turn to the explicit history of the various vessels. The main blood-vessels in an embryo of this length (7 mm.) are well known to us through the papers of Mall (1891),



Fig. 419. — Profile reconstruction showing the arterial system of the head and neck in a human embryo 7 mm. long. (N.T. 28.) fAfter Elze, Anat, Hefte, Bd. 35, Heft 106, Taf. 16, Fig. 3.) S, S, 4, 6, and 6 AB, aortic arches; A. bas., a. basilaris; A. car. ext., a. carotis externa; A. p., a. pulmonalis; A.v.c, a. vertebralis cerebralis; Obi., ear vesicle.


Piper (1900), and Elze (1907) ; the latter 's figures are here reproduced and his description largely followed (Figs. 419 and 420). Three complete aortic arches exist, the third, fourth, and sixth. The first pair, already very weak in the preceding embryo (4.9 mm.), are now entirely atrophied, but both dorsal and ventral end pieces of the second arch are recognizable, the dorsal remnant, in fact, being destined to constitute the trunk of origin of the stapedial artery (Tandler, 1902). The upper end of the sixth arches sends out, between these and the fourth pair, a small vascular fragment, which perhaps represents the persisting upper end of a previous transitory fifth arch. The aorta ventralis in the area of the first and second arches now constitutes the a. carotis ex



Fig. 420. — Profile reconstruction of the same embryo, showing general arterial and venous system. (After Elze, Taf. 15, Fig 2.) X 26.5. A. coe„ a. cceliaca; A. i., a. iliaca; A. s., a. subclavia; A. o.tn., a. omphalomesenterica; Atr. s., atrium sinistrum; A. u. s., a. umbilicalis sin.; D. At., ductus venosus Arantii; V. card, a., v. cardinalis anterior; V.cap.l., v. capitis lateralis; V.extr., extremity vein; V. hep.r.s., v. hepatica revehens sinistra; V.o.m., v. omphalomesenterica; V.om.min., v. omenti minoris; V.mes.s., v. mesenterica superior; V.u.s., v. umbilicalis sin.; V.subc, v. subcardinalis; D.C'uv.s., ductus Cuvieri sin.; 7, 20, 25, 29 SA., segmental arteries; Sin. ven., sinus venosus.


terna which reaches into the region of the upper jaw. The internal carotid artery, after giving off the dorsal rudiment of the second arch, courses headward to give off in the region of the hypophysis a branch which courses toward the brain beneath the optic cup, then above this, a small branch to the latter (a. ophthalmica), and dorsal to the eye, a large branch which apparently supplies the main portion of the fore- and 'tween-brain (a. cerebri ant. et med.). After giving off other branches to the lateral side of the 'tweenand mid-brain, the artery ends in its ramus communicans posterior which appears to continue the main trunk into the basilar artery. The a. vertebralis cerebralis now arises from the first cervical segmental artery, and the preceding hypoglossus vessel has entirely disappeared. The stem of the first cervical vessel, however, has been shifted cranially until it is now opposite the sixth aortic arches, whereas earlier even the hypoglossus artery arose relatively further caudad. The two cerebral vertebral vessels unite in the mid-ventral plane to form the a. basilaris, which extends from the area opposite the vagus nerve to the vicinity of the oculomotor nerve, where it splits into the two posterior communicating rami which connect it with the internal carotids. Both the cerebral and the basilar arteries send off many branches to the hind-brain, some of the branches of the former anastomosing dorsal to the emerging fascicles of the twelfth nerve, so that these fibres appear to go through arterial fenestras. The full number of cervical, thoracic, and lumbar segmental arteries exist and all but the last sacral. The umbilical arteries come off the aorta at the level of the last lumbar segments, and now course lateral to the Wolffian ducts and send each a small branch into the posterior limb (a. ischiadica). The ventral branches of the aorta have been reduced to three main trunks: the a. cceliaca arises opposite the fourth thoracic artery; the a. omphalomesenterica is two-rooted, its upper root coming from a level slightly above the fifth thoracic artery, its lower one opposite the sixth; while the a. mesenterica inferior arises opposite the second lumbar vessel. 27 The veins show several important changes. The proportionately great growth of the head gives a great drainage area for the anterior cardinal vein, which is consequently much increased in size. Its foremost tributary is the paired primitive sinus sagittalis superior on the top of the fore-brain. These are the only tributaries to reach the mid-dorsal plane, with the exception of a very short partly paired one on the roof of the mid-brain. 28 Several tributaries from the first two visceral arches reach the main trunk, while behind the ear vesicle the posterior cerebral (Mall) vein has grown to great proportions. The anterior cardinal, proceeding caudally, surrounds the vagus by a venous ring and then goes under the hypoglossus to join the posterior cardinal trunk. The ling no -facial vein (F. T. Lewis) is now no longer a tributary of the ductus Cuvieri, but joins the cardinalis anterior.


  • A ventral vessel is seen arising from the sacralis media beyond the level of the fourth sacral segmental vessels and supplying the end of the gut where it goes over into the cloaca. Branches of this type from the sacralis media are seen in injections of other mammalian embryos, namely the pig, where they are more numerous and reach further headward.


18 Considerable interest should attach to these mid-dorsal veins of the midbrain, inasmuch as Grosser (1901, p. 322) has demonstrated a pair of veins in this locality in bat embryos where they are retained, in fact, in the adult as the v. longi


The posterior cardinal vein, receiving the same number of dorsal segmental tributaries as is sent out from the aorta and sacralis media artery, drains also the marginal vein of the leg bud and along its entire length receives efferents from the Wolffian body; but the axillary vein now reaches the ductus Cuvieri and will soon indeed be a branch of the anterior cardinal trunk. The subcardinal veins (not illustrated) exist from the level of the tenth thoracic segment caudally and are in frequent communication with the corresponding posterior cardinal. The umbilical veins can no longer be traced to the ductus Cuvieri on either side, and the superficial portion of the primitive vein is only represented by several small stems draining from the body wall into the main trunk just before it plunges into the liver. The left umbilical is by far the larger of the two, and the same is true for the vitelline trunks; the right vitelline indeed has atrophied practically completely, and its previous large pathway through the liver has given way to many sinusoidal paths, whose supplying or portal stem may be called the ramus arcuatus while the corresponding draining or hepatic venule is the v. hepatica dextra. The v. hepatica sinistra still opens independently into the sinus venosus. The main mass of the umbilical blood takes a direct path through the liver in the ductus venosus (Arantii), which receives several small veins from the caudal end of the stomach (Magenvene, Hochstetter, 1893; v. omenti minoris, Broman, 1903). From the liver capillaries a slender vessel grows out into the caval mesentery, the anlage of the v. cava inferior.


tudinales meseneephali, apparently homologous with this vein in reptiles (Grosser and Brezina, 1895) . Grosser attributes the disappearance of these veins in other rnammals to the great overgrowth of the cerebral hemispheres, which, as is well known, are notably small in the Chiroptera. He also calls attention to the fact that Salvi (1897) probably saw the same structure, if we may judge from the descriptions in his paper on the development of the meninges in Cavia and Lepus. Attention may here be called to the fact that the primary head capillary plexus in pig embryos halts in its spread along two parallel mid-dorsal lines in the mid-brain as well as fore-brain, and, just as the medial margin of the former plexus comes to constitute the primitive paired sinus sagittalis superior, so also in some embryos an exactly similar condition transitorily exists on the top of the mid-brain. So that from the careful description oil Grosser and the less satisfactory references of Salvi this evidence may now be added to indicate quite clearly, I think, that a condition resembling the reptilian v. longitndinalis meseneephali exists transitorily in all mammalian embryos, including man.


C. Arteries.


DEVELOPMENT AND FATE OF THE AORTIC ARCHES.


Since the human embryo, like that of all other vertebrates, possesses a row of definite gill bars or visceral arches, separated distinctly, externally by clefts, internally by entodermal pockets or pouches, so also its primitive vascular system is in conformity with this fundamental plan, and strong branches connecting the dorsal and ventral aortae — the aortic arches — each course in a visceral arch (Fig. 421). It has been known for a long time that in all vertebrates above the fishes, — i.e., in the amphibia, the sauropsida, and the mammalia — the number of these arches is five A.d. J.



Fig. 421. — Model of the pharynx and aortic arches in a human embryo 5 mm. long. (After Tandler, Morph. Jahrb., xxx, 1902, Taf. v, Fig. 17.) A. d., aorta dorsalia; C. a., conus arteriosus; J., island; IV, fourth aortic arch; VI, sixth aortic arch.


Within the last three decades, however, it has gradually been shown that in reality six arches exist in these classes, the fifth aortic arch being everywhere an exceedingly transitory vessel. 29 20 In 1886 Van Bemmelen for the first time described a transitory aortic arch found between the systemic and pulmonic arches in embryos of birds and reptiles. A year later Boas (1887), in welcoming this discovery, pointed out its importance in the comparative anatomy of vertebrates. He recalled (Morph. Jahrb., Bd. 7, 1882: Bd. 8, 18S3) that in amphibian larvae, as well as in Ceratodus, Polypterus, and Amia, the four aortic art-lies which occur occupy the third to the sixth visceral arches, the pulmonic artery being given off in each ease by the last pair, i.e., by the aortic arch of the sixth gill-bar. It hence appeared evident that the pulmonic arch was the sixth and not the fifth of the series in all vertebrates, and Boas now predicted the discovery of a transitory fifth arch in the embryos of mammalia, the only remaining class in which it had not as yet been seen. Two years later Zimmermann, as is well known, reported the presence of a fifth arch in embryos of man, the rabbit, and the sheep. Tandler's careful paper, following in 1902, reported traces of the arch in the rat and two very clear examples of it in man, for which he furnished the first figures published. Lehman has described what were


Ziimnemiann (1889) was the first to indicate that there was any tendency to the formation of a fifth arch in man, reporting the separation of the fourth arch into two distinct vessels in a seven millimetre human embryo.


In his article on the development of the head arteries in mammals, Tandler (1902) described two very clear cases of a human fifth aortic arch, neither of which, it may be noted, corresponded to Zimmerrnann 's description, for in both cases the fifth arch took origin from the aorta ventralis and joined the dorsal portion of the pulmonary arch. A diverticulum of the fourth endodermal pouch (postbranchial body) separated the fifth and sixth arches, whereas the fourth pouch lay between the fifth vessel and the fourth arch. Since then other observers (Elze, 1907) have reported the partial presence of this vessel in the same situation. The question of the existence of a true fifth aortic arch was soon seen to involve the identification of the postbranchial body as the fifth branchial pouch. Hammar (1904), now, had described an embryo of 5 mm. (N.T. 20), in which five pouches were present, the fifth {using with the ectoderm of a fifth branchial cleft in the manner typical for these structures. Elze (1907), aware of Hammar 's report, and finding a fifth ectodermal cleft opposite the post-branchial body in an embryo of interpreted as vestiges of the arch in the rabbit and gave a distinct instance of it in the pig. It is important that in some of these cases — e.g., in Tandler's (man) and in Lehman's (pig) — we had also to do with what was apparently a fifth pharyngeal pouch. This structure, the so-called postbranchial body, is not new. It had been known to appear behind the fourth pouch but soon to grow into the latter, with which it had a common opening into the pharynx and of which it now appeared to be a diverticulum. It seemed highly significant also that in the cases which have just been enumerated the fourth pouch pointed towards the ectoderm between the fourth and fifth arches, while the postbranchial body occurred between the fifth arch and the sixth. The whole picture of these interrelations, in short, pointed strongly to their all being serial true branchial structures. In 1906 F. T. Lewis • indicated that the very general acceptance of this interpretation was probably caused by the weight of comparative considerations. He called attention to the ordinary conception of a vessel which could be called an aortic arch having a definite course from the ventral to the dorsal aorta, and emphasized that a fifth arch of this completeness had never been seen, except by Zimmerrnann in the rabbit, where subsequent investigators (Lehman, Lewis) have not been able to confirm him. This fact must be admitted, for even in Tandler's clear cases the accessory arch does not join the dorsal aorta, but instead fuses with the pulmonary arch before this ends dorsally. Locy has emphasized that it seems generally true that the fifth arch is in some way connected with the last pair, in some of the lower classes, in fact, the pulmonic arch appears to have split, — e.g., Lacerta (Peter). Other reports have recently come in affirming fifth aortic arches in other mammals, — Soulie and Bonne (1908) in the mole, Coulter (1910) for the cat, and Reinke for the pig, — (Note on the Presence of the Fifth Aortic Arch in a 6 mm. Pig Embryo, Anat. Record, vol. 4. No. 12, December, 1910) and the evidence is too unanimous to cause doubt that vascular rudiments in the position of a fifth arch occur generally in the mammalia.



7 mm. (N.T. 28), felt no hesitancy in identifying the postbranchial or ultimobranchial body as the fifth branchial pouch. Finally Tandler (1909) has examined a considerable number of embryos bearing on this point and brought together all that has been ascertained about the fifth arch. His conclusions seem to put the question at rest and tc show that in man, very transitorily, in embryos from five to ten millimetres in length, a true fifth arch exists (Figs. 422 and 423, A and B), springing from the truncus aorticus just before the fourth arteries are given off, and coursing dorsally in what is sometimes a distinct fifth gill bar to open into the sixth arch close

4th endodermal pouch, ventral diverticulum



Fig. 422. — Model of the pharynx and aortic arches of a human embryo 7 mm. long. (After Tandler, 1909.) ( Embryo H> of the I anat. Lehrkanzel, Vienna.) to its upper end. In relation with it is a special transitory branch of the vagus nerve (ramus posttrematicus, Elze), 30 in front of it is the fourth entodermal pouch, and behind it the postbranchial body (fifth pouch). The latter is indeed in early stages apparently only a caudal ventral division of the fourth pouch. It is later

30 Ramus posttrematicus der IV Schlundtasche," "E. posttrematicus V," or " R, posttrematicus II des Vagus," given off by the N. laryngeus superior shortly after its departure from the ganglion nodosum and described by Elze (1907) and Tandler (1909) in embryos from 7 to 9 mm. in length. It is usually absent in later stages, although Grosser (1910) believes he has identified it in an embryo 19% mm. (crown-rump), passing through the foramen thyreoideum.




Fia.423 A and B. — Model of the pharynx and aortic arches of a human embryo 9 mm. long (XT. 37).


(After Tandler, 1909.)


incorporated in the thyroid gland (Tandler, 1909, Grosser, 1910), although apparently not contributing true thyroid tissue (Grosser).


The only certain facts which have been established in the metamorphosis of the human arches into the trunks of the permanent vascular system have been incorporated in the diagram of Fig. 424. As far as their actual arch portions are concerned, the first two aortic arches are commonly lost, but the third and left fourth arches are retained, becoming the root portion of the internal carotid and the arcus aortae respectively. On the other hand, both the ventral and dorsal aortae beyond the position of the third arches are preserved, the former to furnish the stem of the external carotid, the latter the second part of the internal carotid



Fig. 424. — Diagram of the aortic arches and their fate in man.


artery; whereas the ventral aorta between the third and fourth arches becomes the stem of the a. carotis communis. The corresponding part of the dorsal aorta disappears, so that now all of the internal carotid blood courses by way of the ventral stem. The sixth arch is lost on either side beyond the origin of the corresponding pulmonary artery, but on the right its proximal portion, between the truncus and the a. pul. dextra, persists and is the root portion of the adult right pulmonary artery. On the left side, however, this proximal portion of the pulmonic arch is apparently incorporated as part of the truncus pulmonis, and the adult a. pul. sinistra consequently is merely the exact analogue of the embryonic vessel (Bremer). 31

31 This subject forms one of the few instances in which a correction is necessary in the conception originally given us by Rathke in his epoch-making monograph on the " Aortenwurzeln und die von ihnen ausgehenden Arterien der Saurier." Rathke, as is well known, represented the right and left pulmonary arteries both coming each from its respective arch in lizards and birds, but for the snakes among


This, then, is the general outcome of the arches, although we are now in the possession of some facts concerning the fate of the first two arches about which nothing hitherto has been known.


Before proceeding to consider details of the changes undergone by the various arches, mention may be made now of several kinds of shifting or growth displacements which affect these vessels and which make it easier to understand the relations which characterize the chief trunks derived from them in the adult. In the first place, as His clearly showed, the place of insertion of the aortic truncus into the anterior pharyngeal wall, whence it is split up into the arches, moves gradually lower down, so that, while at first the arches go off horizontally and even more caudally placed from the truncus, they soon course in an ascending direction from

the reptilia and for the mammalia he showed the two vessels arising from only a single arch, in the snakes the right one and in the mammalia the left one. Rathke's ideas were founded on appearances given by embryos which have passed the earliest stages of origin of the pulmonary artery. His first showed that the earliest human puhnonaries came each from its respective arch, as in the lacertilia, and Bremer has proved that this is a general fact for all the mammalia, and suggested the high probability of its general occurrence, at least in earlier stages, in all air-breathing vertebrates. Bremer's studies have included man, the rabbit, cai, dog, pig, opossum, sheep, guinea-pig, cow, and deer, and, as a result of them, he distinguishes two methods for the formation of the adult pulmonary stem in mammals. In the method occurring most generally (man, cat, dog, rabbit, sheep, cow, deer, and opossum) the original symmetry is disturbed by an absorption of the proximal part of the left arch into the truncus pulmonalis, so that the left pulmonary, artery now rises from the bifurcation place into left and right arches while the right artery comes off its usual distance from this bifurcation place. With the destruction of the distal part of the right arch up to the point of origin of the a. pul. dextra and the eventual atrophy of the corresponding part of the left arch, the adult plan is reached, and this therefore means that we must consider the left pulmonary artery as representing only the original embryonic one, but the right pulmonary vessel has also as its most proximal part the right pulmonic arch. A second method followed in the evolution of the adult mammalian pulmonaries is exemplified by the pig and guinea-pig, in both of which forms the two early pulmonary arteries are joined in a general capillary plexus, the anastomosis enabling one root to serve as a common stem, which in the pig happens to be the left original artery and in the guinea-pig the right. Consequently, in the former animal the blood to both lungs must first traverse the proximal parts of the left arch and left original artery, and in the latter animal the corresponding parts on the right side. Sakurai (1904) has declared that the left artery in the deer moves toward the right past the bifurcation of the truncus pulmonalis to the right arch, but Bremer questions his interpretation, and the case here must rest till an examination of more abundant material in the stages implicated. In the meanwhile, Bremer's work has shown the incorrectness of the conventional diagram in which both definitive pulmonaries are shown as sharing equally the proximal parts of the sixth arches, for in no mammal is this true. Man and most of the other members of the class have a right a. pulmonalis which is of this nature, but an a. pul. sinistra, which is merely the original pulmonary artery of that side, the corresponding proximal part of its arch having been assimilated in the truncus pulmonalis.


the caudally placed root stem. These changes have been described as a " moving down " of the insertion place of the truncus, and are doubtless due to the same phenomena of unequal growth which cause the apparent rapid descent of the heart from its earliest position at the end of the fore-gut. This change takes place in a regular and characteristic way, as Figs. 425, 426, 427 clearly indicate. Originally, when only two arches exist, the truncus may

V. carrli- — 14 « nalis ant. Iv^l

V. urnbilicalis


Sinus reuniens _Sinus reuniens

V. umbilicalis

Vv. omphalomesenteric-;!'


Vv. omphalomesentericse.



Fios. 425 and 426. — Reconstruction of the aortic arches in two human embryos, measuring 2.15 mm. and 3.2 mm. respectively. (After W. His, Anat. mensch. Embry., iii, Leipzig, 1885, p. 1S6, Fig. 119, and Atlas iii, Taf. ix, Fig, 12 and 15.) be described as splitting to send on either side of the gut an ascending and descending limb — the first and second arches respectively. Soon the full complement of arches is present, and the downward progression of the aortic truncus with respect to the gill bars now gives a different arrangement of its arches from the parent stem. Both of the first two arches arise together from an ascending stem, while the third arch courses back practically horizontally from the truncus and the last two come off together from a descending

620 stem. Next an exaggeration of the length and importance of the common ascending stem for the first two arches (the stem which will later constitute the external carotid trunk) occurs and a truly ascending course for the third arch, although the latter has not yet been incorporated in the larger ascending trunk (Fig. 426). In the next changes which take place, the third arch has been carried up in the general ascending trunk (now the common carotid trunk),

V. cardinalis ant.



V. cardinalis post.



V. umbilicali;

Vv. omphalomesenteric^ Fig. 427. — Reconstruction of the aortic arches in a human embryo 4.2 mm. long. (See Figs. 425 and 426.) whereas the fourth tends to course more nearly horizontally, Eventually even the fourth and sixth arches come to have an ascending course.


At the same time that these changes in the arrangement of the arches have been taking place, another of a more general nature has transpired, for not only the heart but the whole system

DEVELOPMENT OF THE VASCULAR SYSTEM. 621 of arches also has moved down toward the thorax. A reliable criterion of this general dislocation is furnished by the relation of the arches to the dorsal segmental arteries, for the latter have a fixed relation to the somites of the dorsal body wall. Before the stage of five millimetres, all the series of dorsal segmental arteries, including the hypogiossus artery, are considerably below the junction place of the sixth arch with the dorsal aorta. By the stage of seven millimetres this place corresponds to the first cervical dorsal segmental, by the stage of nine millimetres to the second vessel, and by the time the embryo has reached eleven and a half millimetres to the sixth or even the seventh cervical segmental, from which trunk the subclavian and vertebral arteries arise (Tandler). This relation is at last almost that of the adult, where the subclavian comes off the transverse portion of the aortic arch.


At the stage of seven millimetres, a splitting of the truncus begins, proceeding from above downward and separating the fourth arches, with the system lying above them, from the sixth ones. The latter then come to have an independent common trunk, — the truncus pulmonalis, — and this, as is well known, is exclusively connected with the right heart, whereas the truncus aorticus is similarly in relation with the left.


Still another growth change in the arrangement of these vessels is to be mentioned. We left the last three arches in a markedly ascending course. Such a course obtains for the pulmonic arches so long as they persist, but after the division of the truncus the systemic truncus elongates much, pushing, as it were, the proximal portions of the third and fourth arches again upward and giving them a horizontal or even slightly descending course (Tandler).


The dorsal part of the right fourth arch now atrophies beyond the origin of the subclavian stem, and this whole segment now constitutes but a branch of the persisting a. anonyma.


A. Carotis Interna and its Branches. — It has already been emphasized that the earliest branch of any of the arches consists in that given off by the dorsal part of the first arch toward the embryonic mid-brain. This persists and is of increasing importance, and when the atrophy of the connecting portion of the dorsal aorta between the third and fourth arches results, it constitutes, together with this part of the dorsal aorta and third arch, the internal carotid artery. The internal carotid, then, consists of three morphologically different portions, — a proximal or root portion derived from the third arch, an intermediate portion consisting of the original aorta dorsalis from here to the first arch, and an end portion which is the earliest branch of the first arches and is the chief supply of the brain. 32

32 Injections of very early bird and mammalian embryos show that the trunk of the internal carotid arterv extending from the first arch distalward is


It is to be noted that, besides the larger internal carotid which is given off from the end of the first arch, the aorta dorsalis also sends several smaller branches toward the hind-brain before the region of the primitive segments is reached, and, when, at length, the latter territory is reached, the dorsal segmental vessels. Those dorsal branches which are in front of the segmental area are very transitory, and attract onr interest chiefly because they represent the first vascular sprouts sent out by the dorsal aorta into the tissues of the embryo in this region and, directed toward the sides of the medullary tube, are directly responsible for the formation of the v. capitis medialis. 33 represented at first by the outgrowth of a plexus of capillaries from that arch (Figs. 393, 394). This plexus spreads over the sides of the early mid-brain first, then over the fore and hind-brains (Fig. 395). Soon out of the several capillary stems of origin from the first aortic arch, one is chosen to become the artery and the remainder perish. Gradually the plexus of capillaries invades the ventral surface of the brain and tends to halt there on either side of a narrow mid-ventral non-vascular strip. In the meanwhile the continuation of the main arterial stem is being evolved out of this plexus in such a way that the carotid, after giving off an a. ophthalmica, appears to have two terminal branches anterior and posterior. The latter connects up with the medial ventral margin of the capillary mesh on each side, and so there come to be in the midventral region two long parallel vessels, the continuation of the posterior terminal branches of the two carotids. This conversion of the medial margins of the ventral capillary mesh here is analogous to the formation of the aorta? from the medial margins of the vitelline capillary plexus. It will be shown that in the spread of the capillary plexus over the spinal cord an exactly similar phenomenon takes place, — that is, the capillaries halt along two parallel lines on either side of the midventral plane. In the cord region also these two plexus margins are converted into two transitory longitudinal arteries, furnished at every segmental point by blood from the segmental arteries and connected headward with the same vessels supplied by the carotid arteries. The whole structure from head to tail has been called by Sterzi the tractus arteriosus primitivus; by De Vriese the primitive anterior spinal arteries. It will be evident from all this that this primitive midventral vessel is the earliest arterial anastomosis between the carotids and dorsal segmental vessels. The second of the dorsal segmentals is the hypoglossal artery, and that part of the anastomosis between it and the carotid is of the greatest importance, for it, according to De Vriese, is the a. vertebralis cerebralis of His; at any rate it is destined to form the basilar artery in the region beneath the hind-brain. Thus the basilar artery is primitively paired and gets its chief supply of blood from the carotids, for the hypoglossal artery cannot figure greatly. Gradually the double basilar is replaced by a single vessel, which is really formed through the development of anastomoses between the two parallel trunks permitting the original left vessel to persist in some areas and the right one in others. This is also what happens as regards the anterior spinal artery. Very soon after the unpaired basilar is produced, its lower source of blood exceeds its upper in importance, and when the cerebral vertebrals are taken over by the cervical vertebrals, the latter vessels are the main supply of the basilar.


83 These pre-segmental branches of the aorta have, of course, another interest, inasmuch as we may be dealing with evidences of a segmentation of the head in front of the occipital somites. Be this as it may, Tandler (1902) has seen a remarkable row of these vessels in the rat. where they seem to arise at regular intervals.


As soon as the region of the somites is reached the dorsal aortic branches are strictly segmentally arranged, — i.e., they course between successive somites. The pair between the first and second somites, however, early atrophy, and the pair situated between the second and third somites and which are in relation with the hypoglossus nerve remain somewhat longer and, as the so-called hypoglossus arteries, constitute the first of the series. In embryos of five mm. length (Tandler 1902, Ingalls 1907) the hypoglossus can be seen giving off a long longitudinal cranial-coursing branch, which headward anastomoses with the a. carotis interna on each side, thus making two long arterial arches. This branch of the hypoglossus artery is the a. vertebralis cerebralis. Later, as has been mentioned, the a. vertebralis cerebralis is taken over by the first cervical segmental artery, and the hypoglossal artery atrophies, and still later, as was first shown by Hochstetter (1890), an anastomosis between the first seven cervical segmentals (aa. vertebrates cervicales) enables the seventh of these vessels to act as the origin for the vertebral artery. De Vriese has pointed out that in all early embryos the carotid, after giving off the ophthalmic artery, may be considered as dividing into two terminal branches, anterior and posterior, the latter of which turns round to anastomose with the a. vertebralis cerebralis and is by far the more important of the two. When the cerebral vertebrals fuse to a basilar artery beneath the hind-brain, the two posterior terminal branches of the carotids consequently join each other in this trunk. This is the condition of the arteries in the head in embryos measuring nine millimetres (Fig. 428). Here the ophthalmic artery is not illustrated, but the carotid is seen splitting into its two terminal trunks, a small anterior and a strong posterior, the latter continued into the basilar. The anterior terminal trunk immediately gives off the anterior chorioidal artery and proceeds as a prominent vessel on the side of the fore-brain, encircling the optic cup from above and meeting its fellow of the opposite side just behind the olfactory pit. This vessel is the a. cerebri anterior, and gives off many rami to the cerebral vesicle, which are later represented by a single (Compare his Fig. 8, p. 302.) De Vriese (1905) mentions their appearance in the rabbit (see her Fig. 28, planehe 16), and for the area in front of the hypoglossus vessel mentions two as being more constant, one at the level of the otic vesicle and the other near the gasserian ganglion. In the human embryo KroemerPfannenstiel (N.T. 3), with six somites, I have found two of these vessels on the left in front of the first somite, and in the Eternod embryo, with eight somites, one behind the region of the first aortic arch, just in front of the second pharyngeal outpocketing ; whereas in the Spee embryo No. 52 there are on each side, although not paired, four of these pre-segmental dorsal branches of the aorta. Finally, Ingalls in his 4.9 mm. embryo distinguished clearly four of these vessels on the left side. The relation of these vessels to the cranial nerves or visceral arches awaits demonstration.



624 trunk, the middle cerebral. The posterior terminal branch of the carotid gives off many branches to the sides of the mid-brain, and these later are also represented by a single trunk, the posterior cerebral. In the next succeeding stages we see an increase in the

A. chorioidealis ant.



A. cerebri ant. et med


A. vertebralis

Fig. 428. — Graphic reconstruction of the arterial system in the brain of a human embryo 9 mm. long. (After Mall, Amer. Jour. Anat., vol. iv, Plate I, Fig. 4.) (Mall No. 163. ) importance of the anterior chorioidal artery (Fig. 429), but it is remarkable that single large stems representing either the middle or posterior cerebral artery are very late in appearing. Mall is



Fig. 429. — Graphic reconstruction of the vessels of the brain in a human embryo 38 mm. long. (From Kollmann, after Mall.) (Mall No. 145.)

of the opinion that we must consider the last-mentioned artery as being represented originally by all the small branches which come off from the carotid between the third and fourth nerves behind and the middle cerebral in front. In older embryos (48 mm. long) these many branches are represented by a large mesencephalic artery and a small true posterior cerebral (Mall) ; in older fetuses the latter branch absorbs the former.


The ophthalmic artery is the first branch of the internal carotid to develop. In embryos measuring seven millimetres it can be seen to course toward the eye, dividing in its mid course into the a. ciliaris longa temporalis and a common trunk, afterwards splitting into the a. ciliaris longa nasalis and the a.hyaloidea. The latter artery pierces the optic cup, courses through the vitreous body, and reaches the posterior surface of the lens in capillaries. The arrangement and size of these branches of the ophthalmic are such that the a. ciliaris longa temporalis appears as the continuation of the main stem, and this is true up to the stage of 20 millimetres at least. The ciliary arteries supply a capillary plexus representing the chorioidea. Dedekind (1908) has reconstructed this simple vascular scheme in an embryo measuring 19 millimetres (Fig. 430 and 431). The hyaloid artery is noted by Dedekind as turning into an arterial plexus before being resolved into the capillaries constituting the tunica vasculosa lentis. Here, then, is another instance of several paths being used by the arterial blood before the reduction to a single path. The hyaloid artery serves as the later a. centralis retina, but no retinal vessels are present till late. The researches of 0. Schulze (1892) had indicated the same fact in other mammals. Versari (1903) has stated, indeed, that the human embryo reaches 120 millimetres in length before the retinal vessels are formed. In an embryo of 33.4 millimetres Dedekind has recorded the a. lachrymalis, aa. ethmoidales, and a. nasofrontalis.


We have as yet only an incomplete record of the development of the eye vessels in man, but Versari has furnished important observations on older stages (beginning with 22 mm.). In the splendid paper by Schultze the older stages in many mammals were beautifully portrayed, and some of the eye vessels in human fetuses of the sixth and eighth months shown. However, only Fuchs's careful study in the rabbit can lay any claim to completeness.


Fate of the Second Aortic Arches. — As a rule, no trace of the first arch is seen in embryos of 7 millimetres and only the dorsal and ventral ends of the second arch are evident. Tandler (1902) has recently declared that in man and other mammalian embryos the dorsal parts of the second arches become the root portions of the stapedial artery on each side. 34 The a. stapedialis persists throughout life in some mammals, — e.g., the rat, — but normally atrophies in man. At the height of

34 Although the recognition of an embryonic artery piercing the mammalian stapes dates back some thirty years (Salensky, 1880), no one had before established the relation of this vessel to the aortic arches.


Vol. II.— 40

626 A. ciliaris longa temporalis

Nervus opticus

Inner lamella of optic cup Outer lamella of optic cup


A. ciliaris longa nasalis A. hyaloidea Point of entrance of the a. hyaloidea in the optic nerve Vasa hyaloidea propria Tunica vasculosa lentis"

Fig. 430. — Left eye of a human embryo 19 mm. long, opened through a horizontal section. X 66. (After Dedekind, 1908.)

Lens

Anlage of the chorioidea

Lens

A. ciliaris longa nasalis

V. ophthalmica superior

Nervus optu


A. ophal mica it

Bulbus Fig, 431. — Left eye of the same embryo seen from the temporal side. X 66. (After Dedekind, 1908.)

DEVELOPMENT OF THE VASCULAR SYSTEM.



627

its development it possesses, after piercing the anlage of the stapes, three branches, which follow the three divisions of the fifth nerve ; these are the supra-orbital, the infra-orbital, and the mandibular rami, respectively. The first of these (ramus supra-orbitalis) leaves the main stem, shortly after the stapes is passed, so that the infraorbital and lower-jaw rami have a common stem (Fig. 432). The infra-orbital division of this stem passes behind the third division of the fifth nerve to gain the second division, which it follows. Later (in embryos of 15 to 17 mm.) the external carotid artery anastomoses with the common trunk for the infra-orbital and mandibular rami, just at the point where these vessels are given off. The infra-orbital ramus gains the outer side of the third branch


Fig. 432. — Profile reconstruction of the head vessels and nerves in a human embryo 12.5 mm. long. (After Tandler, Morph. Jahrb., xxx, Taf. v, Fig. 21.) R. s., R. i., R. to., ramus supra-orbitalis, infraorbitalis, and mandibulars of the a. stapedia; L., a. lingualis of the a. car. ext.



of the fifth nerve by the development of an arterial loop around the nerve and the atrophy of the medial limb of the loop. Soon the original common trunk of the infra-orbital and mandibular rami (which lies above the point of the anastomosis witli the external carotid) becomes surrounded by the auriculo-temporal nerve and we can recognize in it the future a. menmgea media. Xow the stapedial atrophies from its origin to its division place into the three rami, and consequently these branches are then all supplied by the a. carotis externa, the stem of supply for the supra-orbital branch being the old common stem for the two lower branches, in which the flow is now reversed ; this is, as has been said, the middle meningeal artery, whereas the ramus infra-orbitalis is the a. infra


628 orbitalis of the internal maxillary, and the ramus mandibularis, the a. alveolaris inferior. This is clear from the diagrams in Fig. 433.


The place of origin of the stapedial artery and its relation to the stapes identify it accurately with the second visceral arch, but its territory of supply, when its three typical rami are developed, is entirely in the province of the first arch. This becomes intelligible when we know that these rami are later acquisitions of the stapedial, that primarily they arose from the first arch, and were later added to the a. stapedialis. Such, at any rate, is the case in the rat, as Tandler was able to show that the blood supply of the jaws (upper and lower) came originally from the dorsal part, of the first arch. To the stem supplying the jaws, a supra-orbital vessel was added, and then from the stapedial vessel an anastomosis with this common stem developed, whereby the three branches went

R.s

R.i.



R. m


A. m. m.



V. a. t.



A. c. i.



a I) c Fig. 433. — Schemata showing the fate of the a. stapedialis in the human embryo. (After Tandler, 1902.) a represents the conditions present in a human embryo 17 mm. long, b those in one 19 mm. long, and c those in one 23 mm. long. II., second branch of the trigeminus; III. , third branch of the trigeminus; A.m.m., a. meningea media; A.c.c, a. carotis communis; A.c.e., a. carotis externa; A.c.i., a. carotis interna; N.a. t., nervus auriculotemporal; R.i,, ramus infra-orbitalis; R.m., ramus mandibularis; R.s,, ramus supra-orbitalis.


to the a. stapedialis. This early history of the three stapedial branches has not as yet been secured in man, but the facts at present known make it none the less certain that the stapedial artery here has gained the territory of the first arch only secondarily. In man the three branches of the stapedial, instead of being derived from the dorsal end of the first arch, are probably derivatives of the ventral portion of that arch and the aorta ventralis. 38

33 It has been known since the time of Rathke that in many adult reptiles an artery exists which pierces the columella. The same reptiles possess another artery which supplies the upper jaw and courses with the vidian nerve. It would be of the greatest interest if ernbryologieal observations here should establish the origin of the vidian -aceomjimnying artery from the first aortic arch and the columella-piercing vessel from the second arch, like the stapedial of mammals. Evidence that this may be true is furnished by an interesting variation found by Grosser (1901) in a young mammalian embryo (bat). Here the infra-orbital branch of the stapedial artery was not a member of the usual trunk, but an independent branch of the carotis interna, having a definite relation to the vidian nerve, just median to which it coursed. If these homologies, which were suggested by Tandler, are established, then


A. Cakotis Externa. — The trunk of this vessel may be considered the aorta ventralis from the origin of the third arches cranialward. His indicated that the lingual artery was among the first of its important branches to develop, and at 17 millimetres (N.T. 65) Tandler identified the superior thyroid, lingual, and external maxillary arteries. These vessels are, in fact, present at 14 millimetres, when the internal maxillary is also being evolved from the anastomosis of its trunk of origin with the stapedial (Fig. 434). At this stage one also sees a prominent branch of the carotis externa coursing dorsalward. This is the a. occipitalis, having the

A. occipitalis \

A carotis ext. v

A. carotis com.



""• A. lingualis

Fig. 434.



A. thyreoidea % superior \ A. maxillaris ext.



-Graphic reconstruction of the face vessels in a human embryo measuring 14 mm.


Mall collection.)


(No. 144,

position and typical relations of this vessel to the muscle masses. Its proportionatel} 7 great development in these early stages is probably to be explained by its importance as a meningeal vessel.



1. The territory of the first aortic arches in all the higher vertebrates is supplied at first by vessels corning from that arch. The stem for these vessels or one of them may course with the vidian nerve.


2. The territory of the second arch possesses a vessel normally related to the columella (or stapes).


3. The second vessel (stapedial) remains in its original state in the reptiles mentioned, but in the mammals usually annexes the branches developed from the first arch.


4. In adult mammals the stapedial artery secondarily surrenders these branches to the external carotid and atrophies, or, in the cases where is persists, at least loses its mandibular ramus to the external carotid artery (rat), and in some cases also its infraorbital one (bat).



630 At 15.5 millimetres, the chief superficial branches of the carotis externa are evident, the a. auricularis posterior and a. temporalis super ficialis.


Nothing is known of the development of the coronary arteries. Tandler has noted their beginnings in a 17 mm. embryo (N.T. 65).


The only observations known to nie (1901) on this subject are the fragmentary ones of Martin (1S94) and those of F. T. Lewis (1904). Lewis has called attention to the fact that the heart of early embryos is nourished by diverticula of the ventricular lumen which course between the muscular trabecular — sinusoids of Minot, the chief method of nourishment of the myocardium in the lower vertebrates. Later the coronary system supervened and there was a great regression of the extensive sinusoidal system characteristic for the preceding stages. Lewis records the coronary arteries being first recognizable hi rabbits of 14 days and 18 hours.


Variations. — The variations in the great vessels arising from the aortic arch have been known for a long time and could be explained satisfactorily on an


Fig. 435. — Reconstruction of the lung anlagen and their vessels in a human embryo 10.5 mm. long.


(After His, 1887.)

embryological basis ever since the work of Rathke. They have been classified by Krause, for instance, and by so many, following him, that it will not be necessary to consider them here. De Vriese's work has shown the morphological character of the posterior communicating artery, — i.e., this vessel represents the original caudal continuation of the posterior terminal branch of the carotid. Consequently, cases in which the posterior cerebral arteries appear to be supplied by strong posterior communicating vessels, represent merely a retention of normal embryonic conditions, whereas the complete atrophy of the posterior communicating is an exaggeration of normal development. Islands in the course of the basilar are readily intelligible from the original paired nature of this vessel.


Comparative. — In the fish, amphibia, birds, and reptiles the internal carotid arteries are the sole source of supply for the brain, or nearly so, since the vertebrals are unimportant. The carotid in these classes divides into its anterior and posterior terminal branches, and the latter are continuous down the spinal cord with the anterior spinal artery, baring formed the basilar in the region of the hind-brain. This is the simple scheme represented in early mammalian embryos.


The development of the main vessels in the early lung is known to us from the observations of His (1S87). His showed

DEVELOPMENT OF THE VASCULAR SYSTEM. 631 that the two pulmonary arteries are from the first asymmetrical, in that the right vessel passes in front of the so-called eparterial bronchus, whereas the remainder of its course, like the entire extent of the opposite artery (a. pulmonalis sinistra), is behind the bronchial tree (Fig. 435). The pulmonary veins, on the other hand, are placed ventral to the bronchial system, and this relation persists throughout life, giving us arteries separated everywhere from veins by the corresponding divisions of the bronchial tree. 30 Flint (1906) has followed the developing vessels in the lung of the pig, more completely than has been done in the case of any other mammal. The pulmonary veins are reported by most observers as growing out of the sinus venosus before the development of the pulmonary arteries (see also Federow, 1910). In this connection, Flint has suggested that the early appearance of a drainage channel ventral to the pulmonary anlage and the ventral projection of the anlage from the walls of the foregut combine to favor the mechanical establishment of arterial paths dorsal to the organ. These early relations are only repeated in growth, and hence may be regarded as fundamental in determining the architectural interrelations of bronchial and vascular trees in the adult organ. In relation with this is the fact that the eparterial bronchus receives a ventrally placed arterial supply, and that here, consequently, the veins and arteries are accompanying vessels. It seems hardly necessary to refute the error of Aeby (1880) and others who attempted to make the arrangement of the arteries responsible for the form of the bronchial tree. As Flint has emphasized, the arteries are mere passive followers of the bronchi in development, and arise secondarily from the capillary mesh which enveloped a newly formed diverticulum of the bronchus. 36 THE BRANCHES OF THE AOETA.


As has been seen from the preceding description, the history of the development of the arterial system in the human embryo shows that at first two long channels exist — the descending aortae — which course through the entire length of the embryonic body and emerge in the belly stalk without having sent off any branches into the tissues of the embryo. The aortae and their system of branches, then, do not develop like many other vessels of the body, but pursue an elongated unbranched course over an area into which later they are destined to send out a copious supply of arteries. When, as development proceeds, capillaries are finally sent into the embryonic tissues, these sprout from the aorta, dorsally at strictly inter- segmental points, often ventrally and laterally also at such points, but in the case of these vessels usually more irregularly.


The segmental position is strictly observed only in the case of the dorsal branches. These from the first course only in the planes between the primitive segments. The ventral branches, however, are often found arising at more fre 89 Since the above went to press I note that Pensa has given us reconstructions of the pulmonary arteries in two human embryos, 11.5 and 25 mm. long respectively. Antonio Pensa, " Osservazioni sulla morfologia e sullo sviluppo della ai'teria pulmonalis nell' uomo." Boll, della Soc. Med. Chir. di. Pavia Comunicazione fatta nella seduta del 8 Aprile, 1910. Pavia, 1910.



632 quent intervals from the aortic wall, while the lateral branches, except the earliest stages, depart furtherest from a segmental alignment. Both ventral and lateral branches, however, show a tendency to adhere to the segmental plan. 87 Recent investigations on mammals and birds indicate that the branches supplying the limb arise from the aorta at multiple irregular points as a typical capillary plexus (see beyond), but are later segmentally arranged, as is the case in the earliest stages yet seen in man.


The aortic branches fall into three groups or rows, a dorsal row, a lateral row, and a ventral row. At first the dorsal segmentals supply only the central nervous system (the spinal cord and its ganglia), the lateral row, only the Wolffian body, and the ventral row, only the primitive intestine. 38 But of these branches, those which are at first purely neural in their area of distri


Longitudinal anastomoses along the neural tube

v. card. post.



v. subcard. lat

v. subcard.'* medial.



Longitudinal anastomoses along the neural tube

v. card. post.


ramus seg. dors.


ramus lat.



ramus ventralis aorte.



Fig. 436. — Reconstruction to show the branches of the aorta in a human embryo with 23 somites (NT. 7). The reconstruction was made from six successive sections in the mid-thoracic region.



bution come eventually to supply also the body wall with its muscles and skin, and those at first purely nephric to supply also the gut branches which persist,

the adrenals and the sex glands

,T I am aware that Broman, for instance, bases much of bis discussion of the position of the ventral branches and their changes on the supposition of their being primarily segmentally arranged. This, however, is not the case, as my experience with embryos of from six to twenty-three somites clearly proves. Many of the ventral branches are unquestionably as far as possible from a segmental alignment, so that the most which can be said here is that a segmental influence is evident, but expresses itself imperfectly. Later, however, there is a marked agreement with the segmental plan, so that we have conditions analogous to what occurs in the limb buds where stages of a more irregular row of primitive limb arteries are succeeded by those in which these vessels are segmentally arranged.


38 Felix (1910), chiefly on comparative grounds, assigns the primitive function of the intestinal arteries to the supply of the pronephros. There seems, however, little evidence for this in human ontogeny, where these arteries are from the first truly intestinal vessels and where the pronephric rudiments are not in relation with these but with the primitive lateral branches of the aorta.



DEVELOPMENT OF THE VASCULAR SYSTEM.



633

however, supply, as they do in the embryo, the alimentary tract, the organs derived from it (liver, pancreas), and the spleen.


It is interesting to note that Mackay (1889) constructed a hypothetical schema classifying the branches of the aorta in a similar way, some twenty years ago. The main features of Mackay's classification are thus substantiated by development, for, though he confused some secondary with the primary characters of these vessels, he recognized that there were three kinds of them, naming them, from the influence of adult anatomy, the parietal, the intermediate, and the visceral branches.


The ventral branches arise first, owing to early importance of the vitelline circulation, the dorsal branches quickly after them, and, after an interval, the lateral branches. Although Eternod (1898) did not find any of these branches in his embryo of 1.3 mm.




Fig. 437, — Cross sections of injected chick embryos showing the development of the dorsal segmental vessels. A, cross section of a chick of 50 hours (24 somites), showing the loth dorsal segmental vessels; B, a chick 60 hours old; C, 78 hours old; and D, 116 hours old: all in the neighborhood of the 20th segmental vessels. S.A., dorsal segmental artery; P, C, posterior cardinal vein; S.V., dorsal segmental vein; S. C.P., spinal ganglion's capillary plexus; R.B., ventral radicular branch of the segmental artery; S., first extra-myotomal or skin branch of the segmental artery; A. C, a. centralis; S. P., superficial capillaries without the myotome; /., probable intercostal artery.


length, many of the ventral branches and two of the dorsal series occur in embryos with six somites (N.T. 3), while in an embryo with thirteen somites (N.T. 6) many distinct lateral branches can also be recognized. Both ventral and dorsal branches grow out before the primitive aorta? fuse, and consequently when this occurs an accurate apposition of the two aorta? permits these branches to come off in pairs from the single aorta descendens.


Dorsal Segmentals (Neural Segmentals, " Segmental Arteries" (of many authors), Interprotovertebral Arteries (P. Albrecht), etc.). — The dorsal segmental branches of the aorta have often been referred to as the parietal or body wall segmentals, and, inasmuch as they furnish the large well-known intercostal and lumbar arteries, their segmental nature is preserved and recognizable

634 in the adult. These later branches of the dorsal segmentals (i.e., aa. intercostales et lumbales) so far outstrip the primary trunks in growth that in the adult they themselves become known as the branches of the aorta, and the original dorsal segmentals merely


Ramus cutaneus dorsalis medialis Ramus cutaneus dorsalis lateralis

Ramus dorsalis of the anterior branch of the a. intercostalis

Ramus posterior medialis Ramus spinalis Ramus anterior canalis spinalis A. spinalis anterior A. intercostalis

Fig. 438. — Diagram of the behavior of a typical dorsal segmental artery in the human adult. (Founded on Toldt, Spalteholz, Sterzi, and Grosser.)


Fig. 439. — The first dorsal segmental artery in a human embryo with S somites. (Collection of Professor Eternod, videp. 594.) The endothelium is seen growing in the loose tissue of the first intersegmental cleft.


as their posterior branches (rami posteriores). The course of development, however, shows clearly that the reverse is actually the case.


The dorsal segmentals begin to grow out from the aorta at about the time that the embryo possesses six somites (Fig. 410). The number of dorsal segmental arteries increases rapidly, and in embryos in which the extremities are recognizable, almost the whole series is present. The first pair of these vessels between the first and second somite early atrophies, although they are still clearly evident in embryos of 14 and 15 somites (N.T. 7 and embryo Graf SpeeNo. 52). 30 The second pair constitute the vessels which are known as the hypoglossus arteries. These remain in embryos of five mm. in length, but shortly thereafter also atrophy, so that the first cervical pair — i.e., the arteries between the third and fourth somite, which course with the nn. cervicales 1 — are next the first of the series. As Hochstetter long ago showed for the rabbit, and as is evident for man from the Normentaf el of Keibel and Elze, the whole upper six of the cervical dorsal segmentals atrophy and the seventh only is permanent as the trunk of origin of the vertebral and subclavian arteries; this also functions as the root of origin for the eighth cervical and first (or first and second) thoracic arteries by its strong a. inter xo stalls suprema, so that the next permanent dorsal segmental behind the seventh cervical is the second or third thoracic one.


The following table shows the number of dorsal segmental arteries present in several young embryos.



Designation of embryo.


Number of somites.


No. of dorsal segmental arteries.


Probable identity of the dorsal segmental arteries.


Pfannenstiel-Kroemer, NT. 3. . .


Eternod Pfannenstiel III, NT. 6 Graf SpeeNo. 52 Rob. Meyer 300, NT. 7 Broman, NT. 11 G. 31, NT. 14 Chr. 1, NT. 28 6 8 13-14 15 23 ca30 35 40 2 4 6 11 21 23 29 29 Oi, 2 .


Gi, O2J Gi, G 2 Gi, Gjj Gi — G4.


Oi, O2; Ci-CsJ Ti.


', Ci— C$', Ti— T12; Li.


— O2; Ci-Csj T1-T12; Li, L2.


— O2; Ci— Cs; Tr— T12J Li— L5; Si— S3. 5 Ci— C8,' Ti— T12,' L1-L5; Si— S«.



In their simplest form the dorsal segmental arteries consist of single capillary loops which extend from the aortas to the venae cardinales posteriores (Fig. 437, A), yet numerous other capillaries soon sprout out from these loops; and the aortic end of the original capillary loop becomes the dorsal segmental artery and the venous end the dorsal segmental vein.


Inasmuch as the dorsal segmental arteries constitute at first the arterial supply of the spinal cord, their history belongs to that of the blood supply of the cord.



29 The first pair of the dorsal segmental arteries is not generally referred to. Hochstetter (1903), for instance, states that the first pair of these arteries courses with the hypoglossus nerve, as a result of the embryos which he, Zimmermann (1S90), and Piper (1900) had studied. These embryos were so old that the first pair of the segmental arteries had already atrophied.



636

HUMAN EMBBYOLOGY.



With the exception of the brief account by His (1886), this subject has not been followed in detail in man; on the other hand, the main facts in the history have been ascertained for the birds (chick) and the mammalia (sheep, pig) by a series of injections, and the brief description given is based mainly on these.


The single capillary loops which constitute the early dorsal segmentals approach the spinal cord near its ventrolateral angle and the ventral part of its lateral surface. In succeeding stages these loops give off delicate sprouts, which reach the cord at the area mentioned and anastomose with corresponding capillary sprouts given off by the adjacent segmentals, thus forming a longitudinal chain of


Fig. 440. — Successive stages in the development of the anterior spinal artery in the pig. The embryos were injected and the cord dissected in the region of the first three thoracic segments. A, an embryo 8.5 mm. long, B 9 mm. long, C 14 mm. long, D 15.5 mm. long, and E 28 mm. long.



capillaries on the lower lateral surfaces of the cord. These capillaries soon increase, growing over the spinal ganglia and forming a close plexus over the lower lateral surfaces of the cord, which extends dorsally as far as the under edges of the ganglia and their roots. Ventrally this plexus extends to the ventrolateral margin of the cord. Along the latter line sprouts begin to grow ventrally, and the earliest and more important of these, occurring near the chief trunks of the dorsal segmentals, represent the future aa. radiculares ventrales. As yet no capillaries have extended beyond the myotomes. Such are the conditions which occur in mammalian and human embryos until a body length of six or seven millimetres is reached. In the succeeding stages the blood stream in the segmental artery em


DEVELOPMENT OF THE VASCULAR SYSTEM. 637 phasizes in each case two main branches out of the many capillaries, an upper or dorsal and a lower or ventral branch. The upper branch courses just ventral to the spinal ganglion and the dorsal nerve roots, joining the general plexus that more intimately invests the cord just ventral to the line of emergence of the dorsal roots, — a. radicularis dorsalis; the lower branch courses ventral to the ventral roots, extending on to the ventral surface of the cord, — a. radicularis ventralis. In the next changes which occur the most striking feature is the behavior of the capillaries on the ventral surface of the cord. The. plexus which had previously begun to extend there advances from both margins until a line is reached on each side corresponding to the lateral limits of the bodenplatte; along this line they halt temporarily in their spread, thus producing a peculiar and highly characteristic vascular pattern which leaves the middle third of the ventral surface — beneath the bodenplatte — devoid of vessels but its outer thirds covered with a close net. The medial margins of this net are soon somewhat enlarged, constituting two parallel longitudinal vessels, the primitive anterior spinal arteries (tr actus arteriosi primitivi). Very soon delicate transverse capillary bridges cross the middle area which was previously non-vascular (Fig. 440). Some capillary sprouts arising from these primitive anterior spinal arteries push into the substance of the cord and course dorsally, ending usually within the gray matter of the ventral horns. These are the future aa. sulci (Adamkiewicz), or aa. centrales. This stage of double anterior spinal arteries was first seen in the human embryo by His (1886). It is probably most definite and typical for human and mammalian embryos from 9 to 11 mm. in length. His's observations showed it well marked in the human embryo of 10.9 mm. and still apparent in one of 13.8 mm.


The anterior radicular arteries contribute directly to the anterior spinal on each side, and the latter vessel is really to be viewed as merely a particularly prominent anastomosis between these aa. radicales ventrales. In like manner, in later stages, a strong arterial anastomosis develops between the posterior radicular arteries and is known as the posterior spinal artery.


To return now to the general development of the dorsal segmental vessels and their system of branches, we find, at the stage which we are considering, these vessels each possess two chief branches, the anterior and posterior radicular arteries, which are concerned respectively in the formation of the longitudinally coursing anterior and posterior spinal arteries, and which as development proceeds become separated more and more from the cord itself by the formation of the meninges, which (in the adult) they must pierce before reaching the cord.


But besides these two branches of the dorsal segmentals, another soon develops which sprouts out beyond into the skin. This is the representative of the trunk which later gives off both the muscular and cutaneous rami; the former do not as yet exist, so that the vessel may be said to be the ramus cutaneus dorsalis medialis (ramus posterior medialis of Grosser, Fig. 438). Below this another branch of the dorsal segmental now extends out ventral to the anlage of the rib. This, the intercostal sprout, represents the ramus anterior of the adult vessel. Its future great growth makes it the chief portion of the final vessel, but embryology shows plainly that the posterior ramus is the parent, and, again, that of the branches of this posterior ramus, the spinal branch is the primary or parent one and others (rami cutanei et museulares) secondary branches of it. From their origin to the point of division into posterior and anterior rami, then, the intercostal and lumbar arteries represent the original dorsal segmentals, but beyond the latter points they are entirely new and secondary formations. One may compare the above figures of the dorsal segmentals of embryos with the schema which I give in Fig. 438 to represent the adult.


Mall (1898) has shown that in the 16 mm. embryo anastomoses connect all the intercostal and lumbar arteries among themselves

638 as well as with the subclavian above and the femoral below. In this way, then, arise the a. epigastrica inferior and the a. mammaria interna, and along with the rectus, nerves, and ribs shift later into the mid-ventral line (Fig. 441). He thus explains the formation of the superior intercostal artery: "The descent of the heart into the thorax on the inside with the descent of the arm over the clavicle on the outside of the body causes great tension on the upper intercostal arteries, and favors the new formation of blood-vessels in


Fig. 441. — Arteries of the trunk in a human embryo 16 mm. long, showing the formation of the internal mammary and deep epigastric arteries. (Mall collection, 43.) (After Mall, Johns Hopkins Hospital Bulletin", 1898.) a more direct line. This is the reason why the main branch of the superior intercostal is a secondary and direct artery from the subclavian." Whereas the first two intercostals passed dorsal to the sympathetic chain originally, they now pass ventral to it.


Concerning the development of the muscular rami which belong to the dorsal segmentals little is known.


The cutaneous rami, though at one time thought to develop equally and symmetrically (Manchot, 1889), do not do so, as Grosser (1905) has recently been able to show. In fact, the segmental symmetry of these vessels is quite completely destroyed in the adult.


It is entirely probable tbat in tbe early stages of development tbe twigs which represent the blood supply of the skin are arranged perfectly symmetrically and

DEVELOPMENT OF THE VASCULAR SYSTEM. 639 segrnentally. They doubtless correspond accurately with the segmental cutaneous nerve branches. Both, passing out from their source, find their territory of distribution opposite them and at the same level. But the skin does not keep its relation with the skeleton, but shifts over it, dragging, as it were, its nerves and vessels with it. Thus it happens that hi the adult the segmental vessels and nerves no longer supply the skin area opposite them. Since in the thoracic region this shifting is chiefly caudalward, the cutaneous nerves all supply territories lying below their points of emergence from the intervertebral foramina. The arteries, however, though tending to follow the same law, also acquire new connections with the skin territories secondarily opposite them, and accordingly also supply besides their own proper segmental area territory which originally belonged to the adjoining more cranial segments. Such a departure probably does not obtain in the nervous system, where we may perhaps rely on the innervation of a skin territory to reveal its primary segmental position. In the case of the vascular system the departure is doubtless due to the tendency of a blood current to take the shortest possible path — a fundamental law in the development of the vessels. Some others accomplish this shorter path by the employment of anastomoses normally existing between the various cutaneous rami, and so come to course not only downward with the nerve of their own original segment, but also directly outward with the cutaneous nerves of contiguous upper segments and emerge with the latter into the skin. The original segmental skin arteries of these more cranial segments thus vicariously supplied may no longer play any role in the supply of the skin and in this way the number of actual skin vessels is reduced. Another cause, besides this shifting and secondary assumption of a shorter path, operates to disturb a primary segmental symmetry in the skin vessels. This also is fundamental in the development of the vascular system — the tendency of favored vascular channels to annex contiguous ones. Such a tendency is shown to a remarkable degree in cases of certain twin embryos, where we appear to have a contest between the two hearts. In the skin plexus the favored channels supplying this net enlarge at the expense of others, and this may result in the complete assumption of the territories of some three original skin rami by the vessel originally belonging to only one. It is probable that this tendency would operate in the absence of any shifting of the skin even though it is encouraged by the latter, for it is unlikely that exactly equal conditions should obtain in the case of supply of all the segmental skin areas, and a disproportion once established is rapidly exaggerated. This is without doubt the reason why both the posterior rami (it. cutanei dorsales mediales et laterales) of a particular vessel seldom persist, usually the medial rami alone persisting in the upper segments and the lateral rami in the lower ones.


The further history of the anterior spinal artery may be briefly given here. 40 His (1886) had noticed that in the human embryo of 18 mm. the single anterior spinal artery of the adult was finally present, and indicated that its definitive singleness was attained by a medial dislocation and fusion of the two primitive trunks, a process typified, for instance, by the well-known fusion of the two aortse. This view has never rested on any embryological evidence, Kadyi (1889), Hoffmann (1900), and others merely accepting it tentatively, following His. Although such a fusion seems to be actually the case in the elasmobranchs (Sterzi, 1904), in the higher vertebrates, and especially in all the mammalia, a 40 Sterzi has pointed out that the condition of paired anterior spinal arteries or a " tractus arteriosi primitivi," is never developed in the mammals to the degree seen in the birds. In the latter class they form large, much stronger and less transient trunks, — e.g., lasting from the third to the twelfth day in the chick. It is interesting to note that this condition is definitive in the cyclostomes.



640 HUMAN EMBRYOLOGY.


series of more elaborate changes must occur before the single vessel is formed. These changes do not involve a fusion process, but consist essentially in the selection of one of the possible paths offered by the primitive vessels and a plexus which has sprung up between them. The single definitive vessel may thus be unilateral, median, or even oblique in origin (Sterzi, 1904, Evans, 1909). In the first case the adult vessel represents one of the original primitive paired vessels, in the other cases it is formed from the median plexus which connects the two primitive vessels." 8 The single anterior spinal begins to be formed in human embryos when a length of about 15 to 16 mm. is attained. The irregular, " vacuolated " character of the young primitive trunk (Fig. 440, E) betrays its origin from the original plexus, as elsewhere in the developing vascular system.


Variations. — The studies of Kadyi (1889), Burrows, 41b and others show that the form of the adult anterior spinal artery often bears the stamp of its method of origin, being median in some areas but in very many others truly right or left sided. In some areas it even retains its original plexus character (circuli arteriosi medullares), and in others consists of two strong parallel trunks which again unite, — e.g., Kadyi (1889), Taf. 3, Fig. 11.


His stated that the double aa. sulci were later shifted together in the midline, but this does not rest on evidence differing from that for his statement of the fusion of the anterior spinals. Usually, indeed, the aa. sulci or centrales are distinctly separate in man, even in the adult (Kadyi), thus disclosing their original paired origin from the primitive anterior spinals : a thing which Kadyi first discovered in man, Hoche (1899) in the rabbit and dog, and Sterzi has recently shown from many other instances to be the general mammalian plan.


Even in those rare instances in which some of the aa. centrales have a common trunk, this does not arise from fusion of the two original ones, but from the development of an anastomosis between these and the persistence of only one of the two penetrating trunks below the level of the anastomosis, as is normally the case in the birds (Sterzi). (Vide Sterzi's figure, page 311.) The aa. centrales are evident in chick embryos of the 96th honr and in sheep embryos of about 6 mm. In human embryos of 10-11 mm. they form two distinct rows of delicate vessels which enter the cord at the margin of the primitive ventral sulcus and, anastomosing on each side among themselves, produce two vertical or dorso-ventral planes of capillaries. These two rigid planes of capillaries form a striking picture of the internal circulation of the cord at this time.


4 ' a Sterzi was the first to show that the anterior spinal artery usually seen in the adult is only formed after the appearance of a series of anastomoses between the two parallel primitive trunks. The final vessel, according to him, may in some regions be derived from the left primitive vessel and in other regions from the right one, according to chance. The development of the anastomoses between the two primitive vessels permits the branches of that one destined to perish to be taken over by its more successful neighbor. Probably the usual anterior spinal is thus really unilateral in origin. At the same time, however, another plan may be followed in some areas. The anastomoses between the two primitive anterior spinals may become so large and numerous as to completely destroy in places the paired character of the arterial channels of the ventral cord surface and in such areas the cord is nourished by a rather wide median arterial plexus, from which later an exactly median vessel can emerge (Evans).


4 ' b Burrows, M. T.. unpublished observations.



DEVELOPMENT OF THE VASCULAR SYSTEM. 641 This is the earliest method of blood supply of the cord in all the higher vertebrates, a sole exception being made for the urodelous amphibia, in which the first cord vessels penetrate from the lateral surfaces (Sterzi).


The further development of the cord vessels is as follows: Some time after the entrance of the aa. centrales into the cord, other vessels also penetrate it from the lower lateral surfaces opposite the level of the dorsal margins of the anlagen of the ventral gray columns (aa. periphericce). For a while, although both these ventral and lateral penetrating vessels exist, the dorsal two-thirds of the spinal marrow is still non-vascular. The whole lateral sides of the cord and its ganglia are quickly covered with the capillary plexus, but few if any sprouts have ventured on to the dorsal surface ( 7 mm. pig embryos) . Thus the cord presents the remarkable condition of a close capillary investment everywhere save on its upper surface, which is as yet non-vascular. However, this surface is now rapidly covered, at first by delicate transerse capillaries which bridge the gap just as they do at first between the primitive anterior spinals. Gradually then a close mesh is formed here. The gray matter of the cord is better and better supplied by secondarily arising penetrating arteries, which may arise as far dorsally as just beneath the posterior nerve roots (sheep embryos of 10^ mm.). Eventually the aa. periphericae exceed in importance the original aa. sulci, an event which occurs not only in man, but also in the rodents, artiodactyls, perisodactyls, and carnivores, in all of which the peripheral penetrating arteries come ultimately to supply the greater part of the cord substance. In the chiroptera and insectivores, on the other hand, the original ventral segmentals remain always the : chief arterial supply of the cord. The white matter of the cord is always supplied late, it remaining practically non-vascular in sheep embryos until a body length of almost 50 mm. is reached. Gradually there develop on each lateral half of the cord four longitudinal anastomotic chains; the first to arise and more important of these forms at or just medial to the line of exit of the posterior roots (sheep, 50 mm.). This is the posterior spinal artery of descriptive anatomy (tractus arteriosus postero-lateralis of Kadyi), and corresponds to the tractus arteriosus lateralis of most mammals. Next, a similar but weaker anastomosis develops along the line of exit of the ventral nerve-roots (tractus arter. ventro-lateralis) (tractus arteriosus antero-lateralis, Kadyi). Finally, anastomotic arterial chains are established dorsal to the dorsal roots (tractus arteriosus posterior, Kadyi), and opposite the ligamenta denticula (tractus arteriosus lateralis), the latter being peculiar to man and the apes. Of the various longitudinal venous trunks which develop, the order of establishment is similar to that for the arteries, the ventral, lateral, and finally dorsal appearing successively.


Anomalies of the Dorsal Segmental Arteries. — As regards their manner of origin from the aorta, the dorsal segmental arteries show two main types of anomaly. They may (1) either disappear completely on one or both sides, their branches being taken over by the adjacent cranial or caudal segmentals, or they may (2) fuse with the vessel of the opposite side into a single median stem, a process normal to the ventral segmentals (vide infra).


Examples of the first type of anomaly are not infrequent in man, Krause having recorded cases in which as many as four interstitia intercostaliawere supplied by a single intercostal artery. It is interesting to note that such a condition occurs on one or both sides in the normal development of certain fish, amphibia, and birds. The second type of anomaly in which the two dorsal segmentals of one and the same segment fuse to a common stem is also common in man. Ernst has recorded a remarkable case hi which all the intercostal and lumbar arteries arose in this way, — i.e., for each segment from a single median trunk. Broman has found this second type of anomaly occurring in instances in the early embryo (13 mm.), and advances the notion that it occurs through an actual fusion rather Vol. II.— 41

642 than through the atrophy of one of the pair. 42 * Many years ago Krause emphasized that the two places in which this anomaly was commonest were in the lowest intercostal and lowest lumbar regions, and Broman suggests that this is connected with the fact that the aorta? first fuse in the lower thoracic region and that a marked fusion process, normally bringing the roots of the two common iliacs together, occurs in the lower lumbar region. Common stems are normally produced in the ease of some or all the dorsal segmental pairs in some mammals, — Lepus (Ernst), Halichoerus (Hepburn).



Arterial arches, cut off

Aorta deseendens dextra


7th dorsal branch


, _^. Arteria cceliaca primitiva



Arteria omphalomesenterica

Arterise umbilicales Arteria caudalis dextra

Cranial root of a. umbilicalis | Caudal root of a. umbilicalis 21st dorsal branch Fia. 442. — Reconstruction of the aorta and its branches in a human embryo 3.4 mm. long. (After Broman, 1908.) The Ventral, Segmental Arteries. (Gut Segmentals, Yolk Segmentals, "Visceral Circle" [Mackay]). — The first branches to be given off by the aortae, if we except the precocious and immense umbilical arteries, are those which course on to the primitive gut and the yolk-sac. Here the primitive aa. vitellinae were first seen in the human embryo by Mall (1897).


Bischoff (1842) has usually been given credit for the discovery of the row of yolk arteries given off by either aorta; his observations were made on the rabbit.



-° a But see Hochstetter, 1911.


Von Baer (1827), however, had preceded him, for in his " de ovi ruammalium et hominis genesi epistola " (Fig. VII a) he shows some six or seven pairs of yolksac arteries in a young dog embryo.


When the two aortae have met and fused, opposite ventral arteries are quite accurately matched, as is always the case with the dorsal segmental arteries, so that from the now single aortic tube there go off at many places pairs of ventral or gut arteries which are also often accurately segmentally (i.e., intersegmental^) placed.


It should be mentioned, though, that, while this is the case for most of the aorta's length, in its most cranial portion the ventral branches have perished before the aortic fusion has taken place, so that a condition of paired ventral vessels from the single aorta does not ever come about in this region, — i.e., in the territory of the occipital and six upper cerical segments.


The most cranial lying ventral branches are very transitory, and the very first of them have entirely escaped notice until recently. In the Mall embryo No. 391 (Dandy, 1910) possessing seven somites, the ventral or gut branches extend as far forward as the first intersegmental cleft (Fig. 408). By the time the embryo possesses fourteen somites (2.1 mm., Mall, 1897, Pfannenstiel III, N.T. 6) the most cranial ventral branches appear in the region of the fourth and fifth somites. In the embryo with twenty-three somites (Robert Meyer, No. 300, N.T. 7) the ventral vessels opposite the next three caudally lying somites are also in degeneration, so that the vessels near the beginning of the eighth somites constitute the first of the functioning series.


In the Broman embryo of 3 mm. (N.T. 11) (Fig. 422) the ventral vessels opposite the 7th cervical dorsal pair constitute the most cephalic of the series, and this pair is probably the most cranial of the ventral branches to persist long enough for fusion of the aortae to occur in their neighborhood. 42 By the time the embryo attains a length of five millimetres, all of these ventral pairs have given place to single median stems (Fig. 443). Broman (1908) believes this to take place first in the middle of the unpaired aorta and to have proceeded cranially and caudally from this point. In a human embryo of five millimetres which Tandler (1903) has described, all of the ventral pairs have "fused" and there exists a complete series of unpaired or median ventral segmentals from the seventh cervical to the second lumbar segments inclusive. Broman (1908) describes these vessels as representing in each case a fusion of the original segmental pairs, and not, as has been supposed (Thane, 1892, and others), persisting right or left members of the original pairs ; but it is possible, as

42 Whether the oesophageal arteries which Broman and I have seen in quite young embryos are remains of these cephalically lying original vitelline vessels or entirely new sprouts does not permit of determination.



644 Felix remarks from his study of the embryo of 23 somites, that this is often not the case, since here occasionally right members of the ventral pairs were already larger. The question is an open one.


Broman has attempted to explain the normal fusion of the ventral segmentals, in contrast to the persistence of the paired condition which the dorsal segmentals

Aorta descendens dextra


Aortic arch

Truncus arteriosus

n s "E « t r. o T a o a o m


terica ._ superior


A. umbilicalis dextra


j00^f

A. cauda Caudal root Cranial root Fusion gaps 23d right dorsal branch

Fig. 443. — Reconstruction model of the aorta and its branches in a human embryo 5 mm. long. (After Broman, 1908.) The cranial end of the right mesonephros and the position of the metanephric anlage are indicated by dotted lines.



exhibit, by affirming that the ventral vessels are from the very beginning placed nearer each other than are the two dorsal stems. This statement, of course, will not hold, as can be seen from the study of younger embryos than were at his disposal (Fig. 444). The coalescence of the ventral segmentals is doubtless connected with those forces which pull the intestine farther away from the aortic wall to produce the dorsal mesentery.



DEVELOPMENT OF THE VASCULAR SYSTEM.



645

It is quite possible that the seventh pair of ventral segmentals remain longer than those above them just because they function as one of the roots of the cceliac artery. At the stage of five millimetres, although the series of mid-ventral segmentals may be uninterrupted, some of the members of the series are already much exaggerated over the remainder and enable us to recognize them as forming the cceliac and omphalomesenteric arteries respectively (Fig. 445). The former vessel arises by two roots from the seventh and eighth ventral segmentals and, coursing ventrally, forks, the two branches being traceable forward toward the portion of the alimentary canal from which later the stomach and liver are respectively derived. The omphalomesenteric artery is by far the largest of the ventral series, and, while its main trunk is the con


Caudal end of the 3d somite

Coelom

Centre of the 3d somite

ftM*****^'



4th ventral segmental artery

V. urnbilicalis

Yolk-sac opening of the' gut

%

«*



Fig. 444. — Cross section of a human embryo of 7 somites, showing the primitive ventral (segmental) branches of the aorta. The yolk-sac is so spread out that these branches appear as lateral derivatives of the aorta, although later ventral. (After a drawing kindly placed at my disposal by Dr. Walter E. Dandy.) tinuation of the thirteenth segmental vessel, the four ventral segmentals cranial to this also share in giving origin to it, for they are connected with this artery by a series of longitudinal anastomoses. As can be seen from Fig. 445, the omphalomesenteric artery splits on reaching the intestine and surrounds the latter at its junction with the ductus omphalo-entericus, with an arterial ring, before proceeding on its way to its final field of distribution on the yolk-sac. Fig. 446 shows conclusively that the left limb of this ring has atrophied, since the artery now passes entirely on the right side of the gut.


Anomalies. — Sometimes a considerable part of the old omphalomesenteric artery persists in those rare cases of the most primitive type of Meckel's diverticulum. In such cases what is undoubtedly the original artery courses beyond the gait and it? diverticulum to the umbilicus, and a dotprmination of nu which side of the

646 gut the vessel courses will disclose whether the right or left limb of the early arterial ring has persisted. All of the more advanced types of the diverticulum, in which the process is merely supplied by an unusually strong vessel but in which the old trunk cannot be identified with certainty, must be inadmissible for the determination of this point, for the diverticulum is a healthy functioning pocket of the bowel and as such could have secondarily attracted for its supply branches from the vessels of either contiguous wall of the intestine. 43

Ductus omphalo-entericus

A. omphalomesenterica

Ductus Wolffii


7th dorsal segmental artery

A. umbilicalis

Fig. 445. — Sagittal reconstruction showing the aorta and its branches in a human embryo of 5 mm. (After Tandler, Anat. Hefte, Bd. 23, p. 192, Fig. 1.) • Opposite the lower colon, no one of the ventral segmental arteries is especially enlarged above its fellows, and the equal part which all of them play in the nourishment of this part of the bowel

    • It is of interest to note that Allen (1883) some years ago pointed out that remnants of both the a. and v. omphalomesenterica are normally found in the newborn of the cat, dog, and guinea-pig in a strand of tissue which reached the navel.



DEVELOPMENT OF THE VASCULAR SYSTEM.



647

prevents us from identifying any one of them as the a. mesenterica inferior. Nevertheless, in an 8 mm. embryo the latter artery is apparent as the 20th ventral segmental (Broman, 1907).


In the succeeding stages in the life of the embryo, the vessels which we must recognize as the cceliac, superior mesenteric, and inferior mesenteric respectively are all found at successively lower levels on the aortic wall, a fact which is to be correlated with the descent of the intestinal viscera (their territories of distribution) into the abdomen. This highly interesting phenomenon, the so


9th dorsal segmental artery

A. coal.



A. omph.-mes.



A. mes


Fig. 446.



-Sagittal reconstruction showing the aorta and its branches in a human embryo measuring 9 mm. (After Tandler, Anat. Hefte, Bd. 23, p. 197, Fig. 2.)

called "caudal wandering" of the visceral arteries, was first discovered by Mall (1891), and has since been abundantly confirmed and extended by the studies of Tandler (1903) and Broman (1908). The subjoined table shows the position of these vessels in a number of human embryos during the time of their migration (p. 648).


The cceliac artery thus wanders from the seventh cervical to the twelfth thoracic segments, a displacement of some eleven segments, and the superior mesenteric artery almost equally as far (ten segments, second thoracic to first lumbar) ; whereas the inferior mesenteric artery wanders through but three segments (twelfth thoracic to third lumbar). The great change which the levels of origin of the first two vessels undergo, in contrast to the slight one of the third, is readily intelligible from the proportion


648 ately great dislocation which the upper part of the alimentary tract undergoes. All of these vessels usually attain their adult levels by the time the embryo is 17 mm. long.


This shifting of the intestinal arteries is not produced by a displacement of the aorta on the vertebral column, but is an actual

Length of embryo. Position of a. coeliaca. ' Position of a. mes. sup. Position of a. mes. inf.



1 4.9 mm. . .


2 4.5 mm. . .


3 5 mm ....


4 o mm ....


5 6.75 mm. .


6 7 mm. . . .


7 8 mm ....


8 9 mm 9 9 mm . . . .


10 10 mm. . .


11 10.3 mm. .


12 11 mm. . .


13 11.7 mm. .


14 11.7 mm. .


15 12.5 mm. .


16 13.2 mm. .


17 14 mm . . .


18 14.5 mm. .


19 14 mm . . .


20 14 mm. . .


21 15.5 mm. .


22 16 mm . . .


23 16.2 mm. .


24 16 mm . . .


25 16 mm . . .


26 17 mm . . .


27 19 mm . . .


28 19 mm. . .



C. 7 Betw. C. 8 and T. 11 C. 7andC. 8 C. 8 and T. 1 T. 2 T. 5 T. 2 T. 4 T. 4 T. 8 Betw. T. 7 and T.8 T. 6, 7, 8 Betw. T. 7 and 8..


T.9 T.8 T.8, 9 T. 10 T.9, 10 T. 10 T.ll T.ll T. 12 T. 11 T.ll (lower part). T. 12 (upper part) T. 12 T. 12 T. 12 (lower part) .



T. 1,2,3,4.



2 and T. 3... 1,2,3,4,5..


4 and 5 5 and 7

Betw. T. 5 and 7.


T. 4, 5, 6 T. 5, 6, 7 T. 6, 7 T.9, 10 T.9, 10 T.8, 9 T.9 T. 10 T. 10 T. 10, 11 T. 10, 11 T. 11 T. 11 T. 12 T. 12 T. 12 T. 12

T. 12 (upper part) T. 12 (lower part) .


L. 1 L. 1 L. 1

L. 1 T. 12 T. 12 L. 1, 2 L.2 Betw. L. 1 and 2 L.3 Betw. L. 1 and 2 L.2 L.2 L.2 L.2 L.2 Betw. L. 1 and 2 L.2 L.2 L.3 Betw. L. 2 and 3 L.2 L. 2 (lower part) L.3 L. 3 L.3

Observer.



Ingalls. 44 Broman. Tandler. Broman. Keibel and Elze. Elze. Broman. Tandler. Tandler. Broman. Broman. Broman. Broman. Broman. Tandler. Broman. Broman. Tandler. Author. Tandler. Author. Broman. Broman. Author. Author. Tandler. Broman. Author

shifting of these ventral branches when compared with the dorsal branches of the same trunk. 45

44 " Zwischen dem f iinf ten und seehsten Rumfganglion findet sich ein bis an den Darm verfolgbares Gefass, das vielleieht als a. mes. inf. anzusehen ist." (Ingalls.) 43 The exact manner in which this wandering of the gastro-intestinal vessels is accomplished has not as yet been established. Undoubtedly one possible method in early stages is by means of the anastomoses which connect the ventral vessels. This, however, will only account for very early shiftings, for the studies hitherto made show that very soon there may not be a single other vessel between the points of origin of the three chief vessels (e.g., Tandler's embryo K.S.). Consequently other methods have been called on to explain this caudal wandering. These are — 1. That it takes place through the formation of special non-segmental anastomoses between the wandering arteries and the aortic wall below them, with the ensuing atrophy of the older roots. The chief evidence in favor of this view consists in the frequent presence of non-segmental roots of origin for these vessels. The original roots being all supposedly segmental, any non-segmental position for the vessel is explained by the acquirement of secondary non-segmental roots. Such a view overlooks the fact that even in the beginning non-segmental ventral branches are present (see, for instance, the vessels in Broman's Fig. 1, page 646).



DEVELOPMENT OF THE VASCULAR SYSTEM. 649 Regarding the development of the peripheral branches of these arteries in man almost nothing is as yet known. 46 Tandler has identified the a. pancreatico-duodenalis superior in an embryo 13 mm. long (N.T. 57). At 15.5 mm. (Mall's collection, 390) the coeliac axis possesses the following branches: a. phrenica inferior, a. gastrica sinistra with oesophageal rami, a. hepatica with its a. cystica (strongly developed), a. pancreatico-duodenalis superior, and a. lienalis (Fig. 447).


Interest attaches to the development of the ventral branches which the adult aorta is known to send to the (esophagus, especially as to whether these also are descended from the early segmental branches. Some of these aa. oesophageales have moreover been identified in relatively early stages, but they are apparently new formations. 47

2. That it takes place through an active ventral wandering, by which it is understood that the caudal wall at its junction with the aorta bulges itself out, while the cranial wall at a corresponding place is taken up by the aortic wall. There is no evidence for this view.


In discussing the subject it is to be pointed out that the cceliac and superior mesenteric arteries have their roots in an uninterrupted chain of anastomosing vessels, and there is no a priori reason why the vessel functioning as the superior mesenteric in one stage may not subsequently be used as the coeliac channel. As the area of distribution of one of these vessels shifted caudally, the blood stream could adapt itself to a more direct path by the employment of these anastomoses which enable it to come from successively lower segments of the aortic wall.


It seems to me most probable, however, that the identity of the three main vessels is established permanently very early, and that the great shifting is due to an entirely different -phnomenon, — namely, to the unequal growth of dorsal and ventral walls of the aorta. Attention may be called here to the remarkable shifting undergone by the fourth aortic arch, for instance, compared with the dorsal segmental vessels, and yet the arches have not been thought to climb down by special secondary roots, etc.


48 Fransen has studied the branches of the a. mesenterica inferior in two human fetuses between the eighth and ninth month. The six chief branches which he finds going off from this artery he interprets not as the usual branches of the third order, but as original ventral segmentals from the aorta and sacralis media, which subsequently became united through a longitudinal anastomosis (the ascending and descending rami of the a. mesenterica inferior), whereas the root portions die. There is nothing embryologically to establish this claim. These lower ventral segmentals do not exist long enough to leave a permanent trace in the mesenteric plexus. Like the earliest limb vessels they are usually of a capillary nature. The establishment of the inferior mesenteric artery rearranges the whole vascular pattern of its territory of distribution, and the six branches to which Fransen refers came out of this plexus.


" In an embryo of 4.5 mm. Broman has identified three of these vessels risin? from the right aorta opposite the third and fourth dorsal segmental vessels, and reports them in embryos of 10.3 and 14 mm. I have myself seen them in embryos of 10 and 14 mm. In the embryo of 15.5 mm. shown in Fig. 447 they are shown as delicate twigs opposite the sixth and seventh thoracic segments, and have been seen in this location or slightly lower in five other embryos measuring from 19 to 23 mm. (Numbers 229/368, 108, 57, and 382. Mall's collection). In the older of these embryos they were represented by a fairly strong vessel opposite the eighth thoracic segment.



650 A. comm._ post.



R. supraorbi talis (arterise stapediales) A. ophthalmica

A. infraorbitalis


-A. basilaris] A. spinalis £»

A. stapedial A. occipita

A. maxillari A. lingualis A. thyr. bui A.temp. suy A. masdllar?

\ — ! — A. vertebralie A. thyreocervicalis

Rami o3BOphageales a. gastric, sin A. gastrica sin A. cystica A. pancreaticoduoden. sup.


A. epigrastica inf .• A. femoralis A. pudenda interna —

j. L..A. pulmonalii

-4th thoracic, segmental ar

- -Aa. cesophagj A. phrenica inf.


A. coeliaca — A. mesenteries su A. lienalis A. mesenterica inf. -3d lumbar segmental ai A. sacralis media -A. ischiadica

a series of sagittal sections. (No. 390, Mall collection.)

DEVELOPMENT OF THE VASCULAR SYSTEM. 651 As far as I know, nothing has been ascertained concerning the development of the bronchial arteries. In the embryo of 15.5 mm. (Fig. 447) three ventral branches of the aorta are seen to constitute aortic vasa vasorum.


The main branches of the mesenteric arteries are formed very early and can be identified in mammalian embryos well under 10 mm. in length. From the time of the earliest existence of the ventral segmentals, the gut is supplied with capillaries, and in the early embryo these form a close plexus in the tissues of the simple intestinal tube.


The earliest capillaries plexify in a fairly definite plane which corresponds to the future submucosa. This tunic — the so-called " tunica vasculosa " of the older anatomists — contains, as is well known, the chief plexus of intestinal vessels in the adult; there the chief vessels of the intestinal wall are found, and it is from them chiefly that the muscular rami and all of the mucosal rami are derived. This fact finds a better comprehension from the history of the vascularization of the gut wall, for in the submucosa the earliest and hence oldest vessels are found. From this layer of vessels, with the progressive development of the muscularis and the mucosa, there sprout out the rami which nourish these tunics. When the first villi are formed they receive simple capillary loops and sprouts; from the capillary plexus of the older villi, the villous arteries and veins are formed. The increase in complexity of the proper intestinal vessels proceeds from above downward, just as does the development of the intestinal walls and especially the villi; the vessels of the small intestine much precede in complexity those of the large bowel, and the latter portion, for a long time smaller in girth, remains supplied only with a single, simple, submucosal net at a time when the small gut has manifold muscular and mucosal rami.


Anomalies. — The cceliac and superior mesenteric arteries sometimes arise from a common trunk — the so-called " cceliaco-mesenterica," Rathke. This is an entirely normal condition in the Anura, some of the Chelonia and Lacertilia, and some of the Mammalia (PhocaBna [Cuvier], Talpa [Tandler], Echidna [Hyrtl], etc.). The formation of such a trunk has been interpreted as due to the approach and fusion of the cceliac and superior mesenteric arteries (Howes, Klaatseh, Fransen, etc.). Tandler (1904), however, has studied the embryonic development of Talpa, in which this occurs as a part of normal development. He finds a strong longitudinal anastomosis between the various early segmentals of the cceliac and superior mesenteric group. Only one of these early segmentals remains as the permanent trunk, and it has as its chief cranial branch a longitudinally coursing vessel, which is doubtless the old longitudinal anastomosis between the segmental series, the cranial members of which have now degenerated. From this longitudinal vessel the gastric (sinistra), hepatic, and splenic arteries are later distinguished as arising. The main part of the permanent trunk is the omphalomesenteric channel; in this way, then, the anastomosis enables the latter vessel to take over the branches which usually belong to the cceliac. Tandler has applied these findings to explain also the anomalous occurrence of an a. cceliaco-mesenterica in man. If his schemata are interpreted liberally as signifying any mesenteric anastomoses by virtue of which one vessel can take over the whole or part of its neighbor, they deserve to stand as the most reasonable and plausible explanation for these anomalies. It is significant that it is always the stronger vessel — the a. mesenterica superior — and never the weaker cceliac which performs the annexation, a fact in conformity with our general ideas of the method of development of the vascular system. Tandler in fact recognizes a general anastomosis between the branches of aorta in this region, constituting, as it were, a general cceliaco -mesenteric complex. Normally there occurs a later separation of the cceliac and mesenteric systems. Broman, on the other hand, thinks that from the earliest time at which they can be recognized these two vessels with their multiple roots are entirely separate; this is because the human material hitherto explored has not revealed a complete chain of anastomoses between the two vessels, as it has in Talpa. The limitations of method of attack here make it probable that these vessels can not always be seen and that future researches will show them present. If they are not present, another method of formation of a truncus cceliaco-mesentericus may be the correct one; this is the active outgrowth of a wandering root from the cceliac which attaches itself to the superior mesenteric rather than the aorta (Broman).


The rather commoner, longer anastomoses between the cceliac and upper mesenteric arteries are doubtless more secondary developments from the plexus in the primitive mesentery. (In this category are to be placed the cases reported by Aeby, Biihler, Fawcett, Tandler, Thane, Toldt, and others.) The superior mesenteric artery has also been reported as taking over the field of the inferior mesenteric (Fleischmann, 1815), but this is doubtless an anomaly of the greatest possible rarity, because the lower vessel is initially so far removed from the superior one as to be from the beginning a far more effective supply for the bowel which is opposite it.


Lateral Branches. (Nepkric Segmentals, Intermediate Arteries (Mackay), etc.). — Mention has already been made of the occurrence of primitive lateral branches of the aorta in human embryos of 15 and 23 somites (see Fig. 436). The relation of these vessels to the lateral branches of the aorta present in embryos of 4 to 5 mm., and which are now clearly concerned in the supply of the Wolffian body, is not clear, and will not be so until intermediate stages are possessed. I shall discuss here only the latter arteries, which we may designate simply as lateral branches of the aorta or the mesonephric arteries.


His (1880) first observed multiple branches of the aorta supplying the mesonephros in a seven millimetre embryo, and Mall (1891) emphasized the tendency of these to be segmentally arranged in early stages. 48 Broman has recently given a more extended account of them and their fate in a series of embryos, and I follow him.


At first, when the "Wolffian bodies are relatively small, the number of mesonephric vessels is correspondingly small and these 48 Tandler has confirmed this tendency for a segmental arrangement of the mesonephric arteries, but the studies of Broman, Ingalls, Elze, etc., show that many non-segmental arteries exist either from the beginning or as a result of shifting of original ones and we must admit that the metameric arrangement of the Wolffian body arteries is soon completely lost. Hochstetter has called attention to the fact that the mesonephric vessels in Selachians are described as coming from the segmental body wall arteries (Dohrn), and in Amphibia as being true segmental offshoots of the aorta (Semon). He is of the opinion that the corresponding vessels in amniotes were also segmentally arranged in correspondence with segmental mesonephric glomeruli, each of which had its own artery. Actual observations on amniote embryos which will support this have not yet been made.



come from only the middle portion of the aorta (2d to 8th thoracic segments) ; but when, at the end of the first month, the mesonephros reaches its greatest development, it receives many direct branches from the aorta at levels cranial as well as caudal to the original ones. The following table will indicate this :

Length of embryo.


Level of origin of mesonephric arteries.


  • No. of.


mesonephric arteries Observer, on each side.


5 mm 5 mm 7 mm 8 mm 2d to 8th th. segments 1st to 12th th. segm 8th cerv. to 12th th 8th cerv. to 12th th. segm 7 Broman (1908) .


13 Tandler (1903).


14 Mall (1891).


20 Broman (1908).



The last vessels added to the series appear to grow out from the level of the first lumbar to second lumbar segments in embryos of 10 millimetres. These indeed are destined to persist in the adult representatives of these arteries, for all the remainder atrophy by the time the embryo is from 16 to 19 mm. long. When the sex glands and the adrenal arise, they are supplied by branches from many of the neighboring mesonephric arteries.


Gradually the sex gland loses all but a single one of its many arteries, and this is the branch from the mesonephric vessel opposite the second lumbar segment. The atrophy of the Wolffian body permits the entire blood stream in this artery now to supply the sex gland, and thus the a. spermatica interna appears to be a direct branch of the aorta (Hochstetter for mammals, Broman for man). 49 The branches of the mesonephric arteries to the adrenal gland are originally many (6 at least), and come off from the higher members of the series, — e.g., in a 10 mm. embryo, from the mesonephric arteries arising from the sixth to eighth thoracic segments. But eventually, with the relative descent of the adrenal, it acquires branches from the Wolffian body arteries at lower and lower levels. At last in 16 mm. embryos the adrenal arteries are branches of three mesonephric vessels near the first and second lumbar segments. 50 With the atrophy of the Wolffian body, these three adrenal arteries persist and consequently take over the entire blood current, thus appearing as three independent branches of the aorta. Before the adult state is reached, the upper and lower members of the series of three adrenal vessels acquire important secondary con


49 Along with this goes the fact that the recognizable rudiments of the Wolffian body in the adult — the epididymis or epoophoron — are naturally supplied by the sex gland artery.


50 It is to be noted that at this stage these are at last the only mesonephric arteries existing, with the exception of the very last member of the series — that of the second lumbar segment — which sends a branch to the sex gland.



654 HUMAN EMBRYOLOGY.


nections, for the latter comes to supply the permanent kidney (a. renalis), 51 and the former the diaphragm (a. phrenica inferior). These secondary fields for the upper and lower adrenal vessels soon exceed in importance their adrenal territory, and so, in the adult, we only speak of the upper and lower adrenal arteries as small branches of the large renal and inferior phrenic vessels, though embryologically the reverse is the case. The a. renalis soon takes a descending course, and only in the second half of fetal life does it appear transverse. 52 Luna (1908) has shown that the a. phrenica inferior does not surpass its adrenal branch in size until about the seventh embryonal month.


As a result of all observations hitherto made, it may be stated that the permanent kidney in mammalian embryos certainly does not receive any large and readily appreciable arterial supply until its definitive position is reached. Hochstetter has stated that the vv. renales also wait such a time for their development. These facts, however, can not be taken to mean that the renal anlage possesses no circulation during the important early period of its development. For it can be shown, even from ordinary histological sections, that the kidney during this time possesses many small vessels in its walls, and Broman (1907) has recently traced connections between these and the posterior cardinal veins, on the one hand, and with the efferent Wolffian body veins, on the other. 53 This is not the only source of blood for the early metanephros, for injections of mammalian embryos (pig) indicate that its capillaries receive arterial blood from the a. sacralis media (Fig. 448) and inferior mesenteric artery. (See Jeidell, 1911.) Variations. — Supernumerary renal arteries have been known for a long time (Macalister [18831 records a case of seven), but until the embryology is accurately known explanations for their occurrence will be highly speculative, as they have been in the past. From the time of Meckel onward, there have been observers willing to postulate a hypothetical " splitting " of the usual single renal artery to explain this! (e.g., Kolster, recently). However, other observers have stated their belief 81 Hochstetter declares the a. renalis of other mammals to be a direct secondary outgrowth of the aorta, and the same history was described by Hill for the pig. The subject is worthy of reinvestigation in very early injected embryos.


62 Broman explains this by a descending course of the a. suprarenalis inferior at the time the a. renalis supplants it. Formerly these vessels were transverse, but after the closure of the diaphragm he thinks the latter successfully prevents any upward extension of the adrenal, and that adrenal growth from now on consequently pushes down its lower pole together with the a. suprarenalis attached there.


63 From such a finding Broman concludes that the post-cardinal venous blood flows to the kidney and is drained out again into the vv. revehentes of the Wolffian body; this would furnish a renal-portal system for the early metanephros comparable with the renal-portal system so well known in the ease of the mesonephros, and in accord with similar observations made some years ago by Hochstetter on the metanephros of reptiles.



in the derivation of supernumerary aa. renales from Wolffian body vessels, and Bromans derivation of the normal a. renalis from this source makes this explanation of multiple renals the most plausible. The abnormal origin of the renal artery in common .with other trunks is of some interest, inasmuch as we can now explain a large number of these embryologically. The inferior phrenic, adrenal, and sexgland arteries being derivatives of the original mesonephric vessels, all combinations in the origin of the former vessels may be expected. Thus the origin of the a. spermatica interna from the a. renalis is not uncommon, the common origin of a. renalis and a. suprarenalis inferior is normal, and the other adrenal vessels may likewise come from the renal. It is now possible, in view of new observations on the earliest blood supply of the metanephros, that certain types of origin

aorta abdominalis - v. card. post.



v. segmentalis dorsalis a. segmentalis dorsalis

v. segmerrtalisjlorsalis a. segmentalis dorsalis


,a. sacralis media ,v. ischiadica a. segmentalis dorsalis corresponding v. segmentalis dorsalis


v. segmentalis dorsalis a. segmentalis dorsalis

Fig. 448. — Arteries to the permanent kidney in a pig embryo 14 mm. long, after an injection of the living embryo. The arteries in question are the small upwardly-directed branches which arise from the a. sacralis media and the lateral plexus formed by the a. sacralis media. The same plexus is seen to give rise to the aa. segmentales dorsales on each side.



of the renal artery from lower sources — e.g., from the a. mesenterica inferior or a. sacralis media — represent the retention of its first vascular connections when the gland was pelvic in position. There still remain, of course, many remarkable anomalies of all these arteries which indicate entirely secondary shiftings or connections, — e.g., the origin of the a. spermatica interna from certain lumbar arteries. Broman has emphasized that the mesonephric arteries may come off at variable points from the lateral aortic circumference, many of them, in fact, being ventrolateral derivatives. It is easy to understand how, in the latter cases, in further growth the mesonephric artery may come to be incorporated with a contiguous ventral branch of the aorta. The most common instance of this is afforded by the common origin of coeliac and inferior phrenic arteries.


End Bkanches of the Aoeta (Caudal, Lower Limb, and Pelvic Arteries). — In all vertebrates in which the hind limbs are im


656 HUMAN EMBRYOLOGY.


portant, the aorta does not appear to go over insensibly into the a. caudalis, but is rather drained of most of its blood by the mighty iliac branches, which we have come to speak of, in addition to the caudal vessel, as the end branches of the aorta. The simplest arrangement of the aortic end branches is that seen in man, and involves merely a tripartite division" into the two common iliacs and the a. caudalis (a. sacralis media). 54 In many mammals, including man, later shifting makes the sacralis media appear as a dorsal derivative of the aorta and not as its direct continuation, — e.g., in the human adult it almost constantly arises cranialward from the "bifurcation place" of the aorta. 55 In the human embryo we have seen that the tremendous importance of an early placental circulation has "pushed forward" the development of the umbilical arteries so that they much precede of course the appearance of limb arteries.


Studies on early embryos show that the umbilical artery is relatively farther cranial in position than it subsequently comes to be, — i.e., it appears to wander caudally. We have seen that thp primitive umbilical arteries possess many roots of origin from the aorta which are in fact only the caudal members of the general vitelline series (aa. vitelline). 56 64 Hoehstetter has shown that in some mammals, although this plan is originally followed, there subsequently occurs a disappearance of the common iliac vessels, so that the external and internal iliacs arise separately from the aorta (cat). Hoehstetter in 1903 felt inclined to explain this as due to a splitting of the aa. iliaea communes, Broman (1908), by a fusion of the umbilicals down to the point of origin of the external iliacs. Very recently now, Hoehstetter (1911) has subjected the matter to a careful restudy, and comes to the conclusion that the cat's truncus hypogastricosacralis comes through a, wandering upward of the origin of the a. iliacae externas from the wall of the a. iliacae communes to that of the aorta ; a similar thing apparently occurs as regards the a. iliolumbales which wander from the external iliacs to the aorta.


85 Young has attempted to maintain that the umbilical arteries really represent the original continuations of the aorta? which have fused only down to the point of origin of these vessels. He goes over into a hypothetical and poorly founded realm in declaring that the aortae thus bend around into caudal arches comparable with the aortic arches. He explains the a. sacralis media as a secondary branch, being much impressed with its dorsal origin from the aorta at a point cranial to the iliacs rather than at the exact division place. Nevertheless in development the sacralis media goes off at the point of origin of the a. umbilicales, and in addition behaves like the aorta in its position, dorsal segmental branches, etc. Broman explains the definitive origin of this artery cranial to the division of the aorta into its iliacs by assuming that the last part of the aortic stem is formed by a secondary fusion of the aa. umbilicales for a short space at their proximal ends. No evidence exists for this view, and if relative growth differences cannot completely account for the apparent cranial shifting of the sacral artery, we must assume a true wandering to have taken place.


  • In this connection it is of interest that in some mammals the omphalomesenteric artery first appears to take origin from the umbilical by a stem which leaves the

DEVELOPMENT OF THE VASCULAR SYSTEM. 657 In very early stages this caudal migration of the umbilical artery is unquestionably brought about by the caudal growth of the aorta itself together with its intestinal branches, the whole forming a plexus with which the umbilical arteries are constantly in relation and by means of which the blood to them gradually flows in more and more caudally placed ventral branches. Thus, in the Kroemer-Pfannenstiel embryo of 6 somites (N.T\ 3), these vessels arise at about the level of the future seventh or eighth segment, — i.e., the fourth cervical somite. In embryos measuring less than 4 mm. the artery is almost at the level of the first lumbar vessels. It is probable that the single or at most double roots which the a. umbilicalis possesses at this stage are its final ones which belong to the original vitelline series. These roots, however, are themselves displaced or "wander" caudally, so that in embryos of 5 mm. they are found at or slightly below the level of the third lumbar vessels. 57 They do not, however, constitute the definitive roots of these arteries, for, as Hochstetter (1890) some years ago showed for rabbits, the umbilical arteries of mammals next gain a more laterally placed root of origin from the aorta by the development of an anastomosis with the posterior limb arteries, whose origin from the aorta now becomes the root trunk of the umbilical artery, the original ventral umbilical root now atrophying. Hochstetter showed clearly that both ventral and lateral roots for the umbilical may exist for a short time coincidently {e.g., in rabbits of eleven days, two hours), and so form an arterial ring enclosing the Wolffian duct and ccelomic cavity, lateral to which the secondary roots and medial to which the primary roots course. Such a condition can be seen in human embryos of about 5 mm. (N.T. 16) as Keibel and Elze (1908) first reported and as may be seen from latter vessel and courses cranially toward the place where later strong arterial connections with the aorta enable the proper omphalomesenteric artery to displace it. Those are the conditions seen by Ravn (1894) in the rat and mouse, and I can report an almost similar phenomenon in early embryos of the pig. Here injections show that there exists for a time (7.5 to 9 mm.) a strong arterial route for the omphalomesenteric artery which arises from the a. umbilicalis and courses cranially to join the former vessel. These phenomena were quite unintelligible before we were aware, as we now are, that the entire vitelline-umbilical complex of vessels is originally one and the same system.


67 Broman has explained this caudal " migration " of the umbilical arteries by the successive development of " wandering " roots by virtue of which the artery acquires lower and lower connections with the aorta. As evidence of this he points to the double-rooted condition in which the artery may be found. This coincides with his explanation for the descent of the gut arteries. It is to be pointed out that many embryos do not show these multiple roots, and the appearance, even when found, is possibly merely an instance of inselbildungen. Disproportionate growth of the two aortic walls may again be responsible for this dislocation, or we may have to do with an actual active caudal migration of an individual trunk.


Vol. II.— 42

658 Felix 's Fig. 449, drawn from the Keibel embryo. In the embryo of 7 mm. (N.T. 28) only the secondary root is found, and the vessels are at their permanent location (at or slightly below the level of the fourth lumbar dorsal segmentals). 58 In embryos of this age, then, the strong umbilical arteries are found giving off, shortly after their origin from the aorta, a distinct branch, which courses somewhat downward and outward to the posterior limb, where it goes over into a capillary plexus. This is the primary artery of the limb, the a. ischiadica, and, while originally reaching the limb

Median root of the a. umbilicalis

a. umbilicalis


Lateral root of the a. umbilicalis

Renal bud

Fig. 449. — Reconstruction of the a. umbilicalis in a human embryo 5.3 mm. long. (Collection of Professor Keibel, No. 1420.) The umbilical arterj' is seen to arise from the aorta by three roots, a visceral and two parietal. (After Felix, 1910.) tissue without piercing the lumbar-sacral nerve plexus, at length the ventral growth of the latter makes this necessary in embryos of 9V 2 mm. (Elze, 1907).


Soon there also arises, from the upper side of the umbilical artery, the second vessel to the limb, a. femoralis, and we may now designate the umbilical trunk from the aorta to the femoral branch, the common iliac, for what is at first merely a femoral soon gives off the a. epigastrica inferior and other branches and consequently

68 According 1 to the investigations of Hochstetter (1911), they have, indeed, wandered to a position farther caudalward than that in which they are normally found in the adult, for in embryos of this age (6.5 to 10 mm.) the fifth lumbar arteries still usually arise from the division place of the aorta, whereas in later embryos, as in the adult, the aortic bifurcation is " pushed up " to lie opposite the fourth lumbar vessels, so that the aa. lumbales V can no longer be found coming from the aorta directly but are given off by the a, sacralis media. The latter vessel appears to wander cranialward independently, and so comes to arise from the dorsal wall of the aorta rather than at its exact division place; it may even be found giving rise to the aa. lumbales IV.


comes to be the a. iliaca externa of the adult. The remainder of the umbilical trunk together with its a. ischiadica constitutes the definitive a. hypogastrica. Now the ischiadica is soon not merely that vessel, for in the 15.5 mm. embryo it gives off a prominent a. pudenda interna (Fig. 447). The root portion of the ischiadica from umbilical to this division place is consequently probably the great anterior division of the a. hypogastrica in the adult, and after the origin of the internal pudic comes to be the a. glutea inferior before at last the a. comes nervi ischiadici is reached. We are still without any series of observations on the development of the pelvic vessels.


EXTREMITY VESSELS.


For no portion of the vascular system do we stand in such need of a series of well-verified observations as we do in the case of the embryology of the extremity vessels. This field is of profound interest, too, from two stand-points : first, because the developmental history ought to furnish us with a key for the explanation of the manv anomalies which the limb vessels show and which have formed the basis for classic studies on the variation of the vascular system {e.g., Baader 1866, Ruge 1883, etc.) ; and, secondly, because enough has already been learned to indicate that the first arterial tree in the limb recapitulates in a striking way the simpler conditions which are definitive for some of the lower vertebrates (Zuckerkandl, 1894). The subject gains added interest also from another aspect, for from a closer study of the extremity vessels, Miiller (1903) and De Vriese (1902) in recent years have been led to advocate the idea of a capillary plexus ancestry for vascular trunks, in contrast to notions which had previously prevailed. Subsequent research has confirmed this general idea, extending it in some places and restricting it in others, as has already been mentioned. However our exact knowledge of the development of the subclavian tree is still scanty, and there is an even greater dearth of observations in the case of the lower limb.


Arm. — The earliest channels of an arterial source into the anterior limb buds are doubtless capillaries which arise directly from the lateral aortic wall at many points and anastomose profusely in the early limb tissue.


This stage has yet to he described for man, but may be shown clearly by injections of embryos of the chick and duck (Fig. 391). That it also obtains in the mammalia has been recently indicated by the reconstructions made by Goppert (1908) for the early subclavians in white mice (Fig. 450). Thus, as many as eleven of these earliest subclavians have been seen in the birds and five in the mammalia (Goppert). The capillary plexus which is formed by the anastomoses and further extension of these delicate vessels into the tissue of the limb is uniformly distributed in the blastema of the latter, save in a definite marginal

660 zone which constitutes a narrow non-vascular shell of mesenchyma lying beneath the ectoderm. The plexus is drained into the posterior cardinal and umbilical veins through a series of small venules, and later, after the survival of only a single subclavian artery, the well-known marginal vein of Hoehstetter is established.


Very soon after the outgrowth of these early multiple subclavians, changes occur which involve a disappearance of those vessels not arising at intersegmental points, so that the arrangement retained consists of two or more subclavian arteries which are located exactly opposite the dorsal segmental vessels in this neighborhood and are hence "segmental subclavians. " In the mammalia, including man, one of these segmental subclavians is always opposite the seventh cervical dorsal segmental vessel (according to Hoehstetter 's method of counting, the sixth), and others

V. card. C.




Fig. 450. — Reconstructions of the arterial system in the arm buds of embryos of the white mouse, S days old. (After Goppert, Verb., d. anat. Gessell., Vers. 22, Anat. Anz., 1908, p. 94, Figs, la and lb.) may have persisted at segmental points above or below this. 59 Very soon after the establishment of strictly segmental subclavians, these vessels are incorporated in common stems of origin with the dorsal segmental vessels, so that they no longer appear as direct lateral derivatives of the aorta, as was the case earlier, but become strong side branches of the dorsal segmentals.


All the stages just mentioned, however, are passed over by the time the human embryo attains a length of five millimetres, for at this stage only a single member of the early subclavian series remains to constitute the definitive subclavian artery, the vessel of 59 Thus, three segmental subclavians have been seen in the rabbit and mouse, and several cases of two segmental subclavians reported for man. The human ^-ens 16 and 17 of the N. T. possess subclavians from the sixth and seventh — «» 148 in Mall's collection has segmental subclavians from the irst thoracic segments. These observations show the possibility ubclavians in man. — i.e., from the last three cervical and first

DEVELOPMENT OF THE VASCULAR SYSTEM. 661 the seventh segment. It forms now the sole supply of the capillary plexus formerly nourished by multiple vessels and, after a short course to the root of the extremity, is soon resolved into a "spray" of many capillaries. As Miiller (1903) has shown, the main stem of the artery at this stage, while tending to be a fairly strong trunk, centrally located, often shows island-formations in its course, and eventually, before the true capillaries arise, becomes quite plexiform in character (Fig. 451). G0


Arterial island .,---'" \ formation \ i I I


/

Fig. 451. — Arm bud of a human embryo 5 mm. long, showing central arterial net. (After Miiller, Anat.


Hefte, Bd. 22, Taf. 25-26, Fig. 1.)

In the next stage which has been described, that of a 7 mm. embryo in the excellent study by Elze, but little change has occurred. No inselbildungen happen to occur into the proximal course of the artery, nor, apparently, is there any plexiform condition of the artery before the capillaries are given off.


In an embryo of 8 mm. Miiller found the subclavian giving off a branch just before the ventral nerve mass was penetrated; this branch continued for a short distance still medial to the ventral nerve, eventually plunging obliquely through the latter and joining the main stem, which has kept along the lateral side of the nerve; from this arterial loop, the main stem continues along the lateral

00 Within the tissues of the limb, then, the central arterial channel is not everywhere in the form of a single tube, but is rather constituted by an axial arterial plexus from which the capillaries are given off. The same character for this central nourishing channel of the early limb can be demonstrated by injections of the vessels in other mammalian embryos, and may be correctly taken to indicate that for a time the arterial current employs several instead of a single channel out of many available channels open to it by reason of the pre-existing general capillary mesh.



662 side of the nerve, and other fine vessels are given off to course just ventral to the dorsal nerve mass of the limb, as well as ventral to the ventral nerve.


This is evidently the condition occurring still in the 9.5 mm. embryo which Elze (1907) has carefully reconstructed, although the branch of the subclavian given off to continue medially along the ventral nerve does not anastomose with the main vessel, which, as in the previous stage, continues along the lateral side of the ventral mass, especially along the m. medianus; a more dorsally directed branch can be followed along the radial nerve (Figs. 452 and 453).



Arterial branch which pierces the plexus brachialis between n. cerv. 5 and n. cerv. 6. N. cerv.



N. radialis

Arterial branch following radial nerve

N. musculooutaneus *


Cranially coursing branch "Island" in artery

N. medianus Main artery of the limb N. phrenicus Fig. 452.- — Reconstruction of the arteries and nerves of the right arm of a human embryo 9.5 mm. long, viewed ventrally. (After Elze, Anat. Hefte, Bd. 35, Taf. 17-18, Fig. 3.) Some years ago Leboucq (1893) reported that in human embryos of about this age (7 to 11 mm.) the primary vessel of the limb coursed in the forearm between the anlagen of the radius and ulna, and represented the a. interossea volaris. Zuekerkandl had been led to expect this fact by comparative-anatomical studies which indicated that the interossea volaris was the oldest trunk in the lower arm, as well as by embryological observations on other mammalian embryos. His studies, constituting the first researches on the development of these vessels, remain of fundamental value.


Comparative. — Zuekerkandl (1894) thus described the condition of the vessels in the fore limb of rabbit embryos 8.9 mm. long, in which the skeleton was just indicated by mesodermal thickenings. The brachial artery, after accompanying the median nerve in a typical way in the upper ami, is continued in the



DEVELOPMENT OF THE VASCULAR SYSTEM.



663

forearm as a stem lying next the skeletal anlagen, covered by the flexor pre-muscle mass. Just below the elbow, the artery gives off a branch which goes through to the dorsal side of the forearm (a. interossea dorsalis). As the main artery continues to go distally, the median nerve turns away from it to become superficial, leaving its internal interosseus branch to accompany the axial vessel, which may thus now be called the a. interossea volaris. As the main part of the median nerve leaves the stem artery it is supplied by the latter with an accompaniment of fine vessels which continue with it along its entire superficial course to the palm, where they constitute a superficial palmar plexus. The axial artery itself divides at the distal end of the forearm into a ramus volaris, which breaks up to constitute a delicate deep volar plexus next the skeletal anlagen, and a strong ramus dorsalis which supplies the back of the hand. In rabbits somewhat older the fine vessels

Dorsal branch

Branch accompanyN. radialis N. ulnaris ing the n. radialis Arterial ring


/


N. cerv. 6

A. subclavia

N. medianus N. musculo- Main artery cutaneus of the limb

u

Branch directed cranially

Fig. 453. — Vessels and nerves of the same arm (Fig. 452) shown from above. (After Elze, Anat. Hefte, Bd. 35, Taf. 17-18, Fig. 4.) along the main median nerve constitute an artery large enough to begin to dispute the field with the interossea volaris, the a. mediana, while the ulnar nerve has a small accompanying vessel, a. ulnaris. Essentially the same conditions are shown in an 11 mm. cat embryo.



De Vriese has found that in the human embryo of 10 mm. the chief nerve trunks are all accompanied by capillary vessels, 61 and has chosen to represent these as already constituting arterial

81 Injected mammalian embryos show that this is partially true, although the poor material with which De Vriese worked has justly led to the conviction that perineural spaces were confused with true capillaries, a fact which the illustrations accompanying her research leads us to suppose.



pathways. It is doubtful whether these should all be given the valuation which she has set on them, and it must be left to future research to modify or confirm the conception of an already quite complicated arterial system which her description gives us.


The author recognizes at this early stage the a. n. interossea dorsalis, a. n. radialis, a. n. ulnaris, a. n. mediani, and a, n. interossea volaris, the last of which constitutes the continuation of the- axial stem and divides just above the carpus into dorsal and palmar branches, which are themselves in communication by means of a small a. perforans carpi. Four vascular planes are distinguished in the hand, two palmar and two dorsal.


In an embryo measuring 11.7 mm. Miiller has reconstructed the chief arterial system of the limb, and, inasmuch as the nerves and the anlagen of the humerus, radius, and ulna were evident, homologized the vessels present with those occurring in the adult (Fig. 454).





Fig. 454. — Reconstruction of the arteria system of the arm in a human embryo 11.7 mm. long. After Miiller, Anat. Hefte, Bd. 22, Taf. 25-26, Fig. 9.) a. a., a. axillaris; a.b.s.s., a. brachialis superficialis superior; a.b.s.m., a. brachialis superficialis media; a.b.s.i., a. brachialis superficialis inferior; S-, widening of the arterial tube after it has passed through the ventral plexus plate; a.b.s., distal part of the a. brachialis superficialis; a.b.p., a. brachialis profunda; a.r., a. radialis; a.i., a. interossea; a.m., a. mediana; a.u., a. ulnaris; a.a.b.s., a. antibrachii superficialis.


The subclavian perforates the brachial plexus in the usual manner from its ventral side, but the strong branch which, as in previous stages, is given off just before the penetration of the plexus to continue on the medial side of the latter, sends an anastomosing branch through the ventral nerves to join the main vessel. This anastomosing branch joins the main stem at or near the origin of the radial artery from the latter, and on its course toward the chief trunk splits into other branches, as the figure shows. Two of these branches also run into the main trunk, one by piercing the median nerve, the other by going under the same, while another branch courses along volar to the median to anastomose eventually with the median artery branch of the main stem again. In the other limb of the same embryo three strong perforating branches join the part of the main artery medial to the ventral nerve mass with the stem lying lateral to the same. So that in both limbs we are dealing with a rather plexiform condition of the axillary artery. 62 62 Great interest attaches to the arterial plexus formed by the three vessels which penetrate the brachial plexus in this embryo, for it again indicates the employment by the arterial stream of several rather than a single channel from the pre-existing capillary plexus. This transitory plexus axillaris arteriosus of Miiller has also been seen in other mammals (Goppert in the mouse). It by no

DEVELOPMENT OF THE VASCULAR SYSTEM. 665 The main vessel pursues a general course along the radial border of the median nerve to become in the forearm the a. interossea volaris. In its upper-arm portion it gives off, in addition to the a. mediana, a small vessel which joins a chain of capillaries lying in front of the radius anlage (identified by Miiller as the a. radialis). Another branch of the main stem joins correspondingly small vessels lying along the ulnar nerve, and constitutes the a. ulnaris.


In his embryos of 14 mm. Miiller has identified the a. profunda brachii, the a. mediana, a. interossea vol., a. radialis, and a. ulnaris. 63 The main vessels in a 16.2 mm. embryo may be seen at a glance from Fig. 455, in which the lower-arm and hand areas have been omitted.


Mention has already been made of the fact that if, for example, the point of union of the sixth aortic arch with the aorta dorsalis be taken as a fixed point, the subclavian artery appears to wander upward. "Whereas in the embryo of 4.9 mm. the a. subclavia is some eight segmental spaces below this point, in the embryo of 7 mm. it is but six spaces below it, and in the embryo of 11% mm. it is opposite the sixth arch.


The a. mammaria interna and the a. thyreo-cervicalis are conspicuous stems in the embryo of 15.5 mm. (Fig. 447). The a. thyreo-cervicalis courses for some distance in the wall of the jugular lymph-sac in this embryo, and, as McClure has observed the same thing in embryos of the cat, the relation is probably of general significance.


In reviewing the facts hitherto acquired concerning the history of the arm vessels, one must be struck with the need of more careful means constitutes an invariable intermediate stage in the development of the arm vessels, but, as Miiller himself has shown, may occur on one side of the embryo, while the opposite axillary is composed of but a single trunk. Such phenomena may be expected to occur somewhat more frequently in the developing vascular system than in the adult, inasmuch as the increasing blood current exercises a more definite choice to the elimination of multiple paths, but that they may persist even here is shown by the occasional presence of islands in the course of adult arterial trunks.


63 In two 14 mm. embryos Miiller has f ound the main arteiw splitting into two branches which surround the median nerve and fuse again, and is consequently of the opinion that we have here a retention of the arterial paths ventral to the median nerve shown in the previous stage. That this has been the case is strengthened by the fact that the two limbs of the ' brachialis meet again at the place of origin of the a. radialis which is quite an exact correspondence with the place of opening of one of the anastomosing channels shown in Fig. 454. In one of these embryos the artery lying ventral to the median nerve is the larger of the two, while in an older embryo (W. P. 20.5 mm.) it is the persisting one. It seems reasonable to suppose that we are dealing here with instances of a so-called superficial brachial artery, which, as is well known, lies on the volar side of the median nerve, while the normal brachial is dorsal to the latter.



studies here. 64 The reconstructions of Miiller and Elze are our sole possessions in this field. Viewed from a more general stand-point, however, the history of the arm vessels in man certainly confirms the conclusions arrived at some years ago by Zuckerkandl in his studies on the general morphology of these vessels, for in man also the primary artery is an axial stem from shoulder to hand and in the forearm constitutes the later a. interossea volaris. There is also a very general agreement among all observers in the important role played by the embryonic a. mediana. 65 However, there is as complete an agreement in the recognition that at first the volar interosseus is the chief lower-arm vessel, and no support whatever for the idea of Janosik who speaks of the mediana in that primary role.



N. to. A*, u.


Fig. 455. — Reconstruction of the nerves and arteries of the arm in a human embryo 16 mm. long. (After Miiller, Anat. Hefte, Bd. 22, Taf. 27-28, Fig. 6.) The vessel accompanying the radial nerve is the a. profunda brachii (a. nervi radialis of De Vriese). A. a., a. axillaris; A.i., a. interrossea; A.m., a. mediana; A. r., a. radialis; A. u., a. ulnaris; A", m., n. medianus; A", m. c, n. museulocutaneus; N. r., n. radialis; A', u., n. ulnaris.


Comparative. — The a. interrossea volaris with a. perforans carpi is the chief vessel of the forearm in the adult in amphibia, reptilia, and in Ornithorhynchus among the mammalia (Zuckerkandl). It is also apparently the plan in the embryos of all the mammals. (Zuckerkandl, rabbit, cat; Hochstetter, Echidna; Grosser, bats; De Vriese, calf.) In very many mammals the chief definitive arterial stem is the a. mediana (marsupials, edentates, most carnivores, bats, etc.). In the primates its territory is taken over by the ulnar. A vessel accompanying the ulnar nerve, hence an a. nervi ulnaris, occurs in adult amphibia and reptiles and apparently constantly in the embryos of mammals. In the adults of the latter class the artery is not, as a rule, important and may be lacking entirely (most ungulates). A vessel which can be designated the radialis is not of general occurrence till the mammals are reached, and in the majority of these is a superficial radial. It comes to possess its deep volar territory in the higher mammals, but its proximal end is still superficial (really the superficial brachial here) in many of the primates, as Bayer has well shown.


M Very recently Goppert (1910) has supplied us with the history of the development of the arteries in the arm of the white mouse, an account which is by far the most complete we possess for any mammal.


55 The observations of De Vriese even indicate that this vessel is not finally displaced from the hand until the embryo reaches almost 30 mm. in length.



DEVELOPMENT OF THE VASCULAR SYSTEM. 667 Variations. — Many of the variations of the arm vessels must remain uncertain in origin until we possess a well verified series of observations on their embryology. There can be no doubt, however, that Miiller has demonstrated the manner in which a superficial brachial may arise, for arterial channels are retained on the ventral side of the median nerve in most of his specimens. It may be pointed out, also, that eases of persistence of great median or even volar interosseus arteries (Baader) are unquestionably survivals of embryonic conditions, and we may have all possible degrees of variation in the part taken by these vessels in the supply of the hand (Schwalbe and others). Krause pointed out that high origins of the radial or ulnar arteries usually involved a superficial course for the proximal part of these vessels, a fact which may be explained by the retention of a brachialis superficialis inferior. Attention may also be called to the very ingenious series of schemata which Miiller lias constructed to explain the lower-arm arterial anomalies, but until more is learned of the normal history here, we can not venture to present satisfactorily founded diagrams for anomalies.


Arteries of the Lower Limb. — In human embryos measuring from 5.5 to 7 mm. and shortly after the umbilical arteries have acquired their secondary, more lateral, stems of origin from the aorta in the neighborhood of the fourth or fifth lumbar segments, there can be seen going out from these vessels on either side, a small artery which penetrates the tissues of the posterior limb bud (Fig. 420). When the nerve-plate for the lower limb grows out farther, it surrounds this vessel, so that the extremity artery appears now to pass through it, just as is the history with the subclavian artery and the brachial plexus. Later the ischiadic nerve joins this vessel and it may consequently be identified as the a. ischiadica.® 6 Probably injections of earliest stages here would show that the a. ischiadica is really only the exaggerated member of a series of vessels, which originally supply the limb tissue, as is the case with the upper limbs.


This vessel (a. ischiadica) forms a central or axial nourishing channel for the early leg bud, just as is the case with the subclavian and early arm bud. Leboucq (1893) first called attention to the fact that the primitive blood supply of the hind limb consisted in a single axially-coursing artery, the a. ischiadica, which, as soon as skeletal elements could be recognized, continued to course in the lower-leg region between the anlagen of tibia and fibula, and ended chiefly as a strong branch which perforated the interspace between the elements of the first tarsal row, to reach the dorsum of the foot. Lately De Vriese 67 has confirmed this.


88 It is to be noted that in mammalian embryos, where the history of the leg vessels has been followed more carefully, the a. ischiadica is primarily a branch of the aorta, and its proximal portion serves later as the stem of origin for the umbilical arteiy when the latter abandons its ventral roots (Hochstetter, 1890). The origin of the a. ischiadica from the aorta has not yet been observed in man.


87 De Vriese has considered the history of the leg vessels in man. I will not, however, detail her account, for reasons given above in the account of the arm vessels.



668 HUMAN EMBRYOLOGY.


It may be well to refer here to the important previous observations of Zuckerkandl (1894-95), who described the leg arteries in a rabbit embryo of 7.7 mm. somewhat as follows : The a. ischiadica is continued in the lower leg as a strong axial vessel next to the skeleton. It sends two perforating branches towards the side of the limb, the upper of which probably corresponds to the a. tibialis ant., while the lower supplies the dorsum of the foot. The distal end of the axial vessel supplies the depths of the sole. Fine vessels accompany the posterior tibial nerve in its lower course, and in embryos of 13.5 mm. these constitute a distinct artery, a branch of the axial vessel. The further history in this animal disclosed the a. saphena (from the a. femoralis) taking over the posterior tibial trunk.


The supremacy of the a. ischiadica in the supply of the extremity is soon disputed by the appearance of a new vessel, the a. femoralis, which in the embryo of 15.5 mm. (Fig. 447) is already the chief vessel in the limb. The femoral soon gains all the branches of the a. ischiadica in the territory of the lower leg {'e.g., tibialis posterior et anterior), by anastomosing with the ischiadica near the knee; we know the a. ischiadica of the adult only as the stem portion of the a. glutea inferior. 6S This ontogenetic history of primary and secondary vessels for the human leg is closely paralleled by the vessels found in an ascending vertebrate series, as Zuckerkandl showed.


Comparative. — The a. ischiadica is the chief vessel of the thigh in the adult for amphibia, reptilia, and the birds, yet the femoral in the latter class may attain quite an area of distribution, and in some {e.g., Spheniscus.) even behaves as in mammals by taking over the chief rami of the a. ischiadica and constituting the chief limb vessel (Hochstetter). On the other hand, among the mammalia the atrophy of the ischiadica is the ride. Yet it may persist in part, as, for example, forming the a. tibialis anterior of bats (Grosser, 1901).


The appearance of an a. ischiadica in the embryos of all mammals was indicated by the observations of Hochstetter and Zuckerkandl. The chief lower-leg portion of the a. ischiadica in adults in the amphibia, reptiles, and birds behaves exactly as it does in the early stages of the embryo of man, namely, courses between the tibia and fibula and supplies the dorsum of the foot by means of a large perforans tarsi. Other stages in the ontogeny of man's leg vessels are found definitive in various mammals, e.g., the stage in which a distinct superficial plantar arch or plexus exists, as well as a deep one. This is the case in most apes, as Popowsky has shown, and is lost in the anthropoids, where, as in man, the lateral plantar artery is larger than the medial and the deep plexus practically the only one present.


Much interest attaches to the saphenous artery. The earlier work of Zuckerkandl emphasized the very general occurrence of this vessel in all the mammalia/' 9 and led him to declare it the oldest (phylogenetically speaking) branch of the 68 According to Hochstetter's (1S91) investigations on mammals the a. comes n. ischiadici does not appear to be a relic of the old ischiadica, although this assumption is made by most authors. De Yriese describes the lower leg portion of the original axial artery (a. n. interossei cruris) as becoming the a. peronea of the adult, giving over all of its important branches in the territory of the foot to the a. tibialis anterior.


19 With the exception of Bradypus bidaetylus, Lemur catta, and man, in which it is much atrophied.



DEVELOPMENT OF THE VASCULAK SYSTEM. 669 femoral. In its lower portion this artery usually takes over the dorsalis pedis artery, or the primary tibialis posterior, or both, in which latter case it constitutes the chief or 011I3- vessel for the supply of the foot. The vessel retains its importance in the primates, — e.g., in Cebus, where it supplies the entire foot. Popowsky has recalled the anomalous occurrence of this vessel in man and reported two interesting cases in which the a. saphena was large, in both cases anastomosing with the posterior tibial artery and in one case in addition with the dorsalis pedis. He has again called attention to the frequent great development of this vessel in the monkeys, where, even in the anthropoids, it supplies the dorsalis pedis. Popowsky, evidently much influenced by this, states his belief that this vessel must play a prominent role in the development of the leg arteries of man. There is no evidence, however, that such is the case. The work of De Vriese indicates there is apparently no necessity for the recapitulation of a stage in which the saphenous functions as the chief artery of the lower leg. In the reworking of this field, nevertheless, great interest will attach to the re-examination of the embryonic importance of this vessel, for the reasons above given.


Variations. — Dubrueil, Krause, Ruge and others have described cases in which the a. ischiadica was the chief vessel of the limb in man, which is quite evidently a survival of embryonic conditions. The occurrence of an a. saphena magna, following the saphenous nerve, has already been mentioned, the first case having been observed by Zagorsky in 1809. Normally this vessel probably reaches the lower third of the leg, for in well-injected subjects I have traced it this far, as Hyrtl first did. Krause and more recently Salvi report cases where an artery accompanies the n. cutan. suras lat. This corresponds to an embryonic vessel seen by De Vriese at the peroneal side of the leg in the 13 mm. embryo, but it usually disappears entirely. Cases in which the a. peronaea instead of the tibialis ant. supplies the dorsum of the foot are not rare, and represent again the embryonic picture where the axial artery behaves normally thus. Most interesting are cases in which a perforans tarsi persists, joining the dorsalis pedis with the deep plantar vessels. In the adult also a superficial plantar arch occasionally occurs, as Krause, Gegenbaur and others mention.


D. The Development of the Veins.


1. The venous types.


2. The ground-plan of the young venous system.


3. Transformations of the vv. umbilicales et vitelline.


4. Transformations of the vv. cardinales anteriores.


5. Transformations of the w. cardinales posteriores.


6. The development of the veins of the body walls.


7. The development of the veins of the extremities.


1. THE VENOUS TYPES.


In the adult, as has been recognized for a long time, the veins tend everywhere to follow the arteries, — i.e., the majority of the veins are w. comites. In the embryo, however, it is possible to satisfy one's self that this is not the primary arrangement, for. if one studies carefully the developing vessels in any area, it will be seen that the earliest arterial and venous trunks are separated from one another so as to stand in reciprocal relation as regards the general capillary bed. Should this primary separation of

670 HUMAN EMBKYOLOGY.


arteries and veins be perpetuated as the vascular trunks continue to grow, we have the plan which obtains, for instance, in the circulation of the- brain or lung, where larger arterial and venous vessels instead of coursing together are arranged so as to stand opposite one another. As a rule, however, as development proceeds the main vascular stems are found coursing together, — i.e., the veins are true w. comites. We have to recognize, then, tivo types of veins, primary and secondary veins, primary veins standing opposite or alternating with the arteries and trunks, secondary ones coursing in company with the corresponding arteries. 70 Venae comites, which are, then, always later formations, may arise either as a result of shifting of primary trunks in growth or entirely de novo. 11 Splendid examples of the persistence of primary veins are furnished by the great subcutaneous veins of the limbs and trunk (v. basilica, v. saphena, v. thoraco-epigastrica). These are in fact remains of the early border veins of the extremities and of very early body wall trunks and it may hence appear more reasonable why they possess no corresponding accompanying arteries.


2. THE GKOUND PLAN OF THE YOUNG VEXOUS SYSTEM.


If now one turns to the details of the developing venous system in man, it will be recalled that the remarkable precocious development of the chorionic circulation gives us the vv. umbilicales at stages much earlier than obtain in the mammalia generally. In embryos of 6 somites (N.T. 3) we can also trace clearly the vv. vitellines, and it can be seen that in their terminal portions the umbilical veins join the heart by receiving the vitelline veins and coursing now as a common vitello-umbilical trunk. 12 At the margins of the anterior intestinal portal, this vessel turns inward, courses in the mesial wall of the pleuropericardial passage, and in the mesodermic tissue ventral to the foregut anastomoses with its fellow of the opposite side to constitute the sinus venosus. The latter is at first situated in front of the first somite (Mall embryo 391, with seven somites), but in the fifteen somite embryo (Graf Spee No. 52) is opposite the body of the first somite, and in the twenty- three somite embryo (N.T. 7) is opposite that of the sixth (Thompson, 1908). In this last stage there open into the sinus

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


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


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



DEVELOPMENT OF THE VASCULAR SYSTEM. 671 the anterior and posterior cardinal veins by means of a ductus Cuvieri, but earlier, when the sinus lies more crarfialward, the anterior cardinal vein joins the common vitello-umbilical vein (embryo of fifteen somites). The intermediate stages are not known in man.


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


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


3. THE TRANSFORMATION OF THE UMBILICAL AND VITELLINE VEINS.


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


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


The umbilical veins next gain connections with the liver sinusoids and eventually lose completely their early superficial course in the region between liver and heart, a fact first noted by H. Rathke (1838). 73 The umbilical blood is now poured into the liver channels, the largest of which is the old direct path of the right omphalomesenteric to the corresponding horn of the sinus venosus. In the mean time the two vitelline veins have anastomosed with

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



672 each other by cross connections, which go, first ventral, then dorsal, and again ventral, to the gut tube and so form two venous rings around the duodenum, as may be seen from Fig. 456. 74 The middle or dorsal of these anastomoses receives the vein from the intestine, the true mesenteric vein.


His pointed out that the usual fate of these venous rings involved always the atrophy of certain limbs and the persistence of others in such a way that an S-shaped course is now described

Ductus venosus Arantii

Junction between the ductus Arantii and the end piece of the left yolk vein

Sinustvenosus, right.Lorn

V. omphalo mesenterica dextra

V. umbilicalis dextra


Sinus venosus, left horn

V. omphalomesenterica sinistra

Cranial anastomosis of the vitelline veins

Middle anastomosis of the vitelline vein

Right vitelline vein

Caudal anastomosis of the vitelline vein

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


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


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



DEVELOPMENT OF THE VASCULAR SYSTEM.



673

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


Venae revehentes

Ductus venosus Arantii Pane. d. Venae revehentes

Cranial end of the v. umbiliealisdextra .



Stomach - -_

Vense advehentes

Ductus choledochus V. umbilicalis dext


Cranial end of the v. umbilicalis sinistra

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

Li ver

V. umbilicalis sinistra

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



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


When, with the growth of the right lobe of the liver, the intrahepatic course of the right vitelline becomes shifted so as to constitute a somewhat circuitous route, a new direct one to the sinus venosus is formed; this is the ductus venosus Arantii. Mall's researches show that the former intrahepatic course of the right vitelline does not completely atrophy without a trace, but leaves representatives in the form of its end, which drains into the sinus venosus, and its first portion, which leaves the umbilical vein, for these are now incorporated as parts of the supplying (portal) and draining (hepatic) systems of the liver, and become respectively the ramus dexter vena? hepatica? and the ramus arcuatus (et descendens) vena? portae. At this stage, then, we have for both of Vol. II. -43'

674

ill MAX EMBRYOLOGY.



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


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


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


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


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


ft ha- been pointed out that at the stage of 4.9 mm. the dorsal anastomosis between the vitelline veins receives the mesenteric vein draining the intestine. After the 8-shaped common vitelline vein

DEVELOPMENT OF THE VASCULAR SYSTEM.



675

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


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


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



676 HUMAN EMBRYOLOGY.


4. THE TRANSFORMATION OF THE ANTERIOR CARDINAL VEINS.


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


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


area ; the former portion lies close at the sides of the hind-brain and should be known as the v. capitis medialis (Grosser, 1907) ; the latter is situated more laterally and is the true cardinalis anterior. 77 Both portions of the primitive head vein are in fre 77 Grosser first separated these two portions of the primitive head vein, which occur in all vertebrates, and called attention to the fact that only the caudal part is homologous with the posterior cardinal and hence merits the name cardinalis anterior. He remarks that the cardinals are probably especially related to the segmental excretory system and that the anterior cardinal is likely evidence of the former cephalic extent of this.



DEVELOPMENT OF THE VASCULAR SYSTEM.



677

quent connection with the aorta by means of numerous small direct branches, the v. capitis medialis by means of dorsal presegmental arteries, the true cardinalis anterior by means of the dorsal segmental arteries as well as by direct lateral branches of the aorta. Later all of these aortic offshoots atrophy, and the chief source of the blood drained by the primitive head vein is supplied by the a. carotis interna. When the anlagen of the cranial nerves first appear, they are found lateral to the vena capitis medialis, but in later stages, as Salzer (1895) first showed, the vein is gradually shifted lateral to the nerves by the formation of channels which course on the outer side of the latter, and the v. capitis lateralis thus produced gives us a secondary, wholly lateral, head vein.



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


(After Mall, 1905.)

(Mall No. 163/

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



n The v. capitis medialis iu the region of the fifth nerve is retained to become the sinus cavernosns of the adult (Mall), but otherwise the early medial head vein leaves no trace of its existence. The v. capitis lateralis is entirely without the skull, or, more accurately, leaves the skull with the seventh nerve to empty ts blood into the internal jugular vein, and so it takes no part in the formation of the permanent head sinuses, although its chief tributaries do so, as Mall has shown in the following way. At the stage of which we are speaking, the v. capitis lateralis possesses three main tributaries, the anterior, middle, and posterior cerebral veins respectively (Mall). The first of these drains the eye (v. ophthalmica) and cerebral hemispheres as well as mid-brain; its most cephalic extension conrses on either side of the mid-dorsal


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


(After Mall, 1905

Mall No. 109. 1

line in the region of the fore-brain and constitutes the anlage of the erior sagittal sinus, thus primitively paired. The middle cerebral vein drains the anterior part of the hind-brain (cerebellum) and joins the main trunk between the fifth and seventh nerves. Since the v. capitis lateralis leaves the skull in company with the seventh nerve, it is apparent that through this foramen the venous blood of the fore-brain, mid-brain, and cerebellum is drained. The last tributary of the lateral head vein joins it behind the otic vesicle, leaving the skull through the embryonic jugular foramen (v. eerebralis posterior). This posterior cerebral vein drains the remainder of the hind-brain (medulla) and first portion of the cervical cord. As the anterior cerebral vein extends forward to the top of the cerebrum, so also the posterior cerebral reaches the mid-dorsal region of the hind-brain (Pig. 464).


Xow anastomoses develop between these three primitive cerebral veins and the v. capitis lateralis atrophies, so that not only

DEVELOPMENT OF THE VASCULAR SYSTEM. 679 the hind-brain blood but that of the entire brain is drained out through the foramen jugulare, and the old anterior exit with the n. facialis disappears. 78 The anastomoses which develop between these three primitive brain veins begin the changes that convert these to the head sinuses. The blood from the sinus sagittalis superior is no longer returned by way of the anterior cerebral vein, but courses dorsally by means of a new anastomosis which links it to the upper end of the cerebralis media. Very soon, though, an anastomosis is carried still further caudally, so that the blood now enters the posterior cerebral vein, which leaves the skull through the jugular foramen. This last and most important anastomosis forms the


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



680 HUMAN EMBRYOLOGY.


original cerebraiis media is probably incorporated to form the superior petrosal sinus, but the inferior petrosal sinus is a later formation. 79 " 1 The v. jugularis externa is a secondary venous channel which in man, as in the mammals generally, appears relatively late (embryo of 16 mm., F. T. Lewis, 1909; see also Schawlowski, 1891). We possess as yet no connected history of the vein for man.


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


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


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



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


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



DEVELOPMENT OF THE VASCULAR SYSTEM. 681 5. TRANSFORMATIONS OF THE POSTERIOR CARDINAL VEINS.


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


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


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


For the details of this change we are indebted mainly to the investigations of F. Hoehstetter and of F. T. Lewis on the rabbit. A complete account for man,

81 It may again be emphasized that in the beginning the posterior cardinals receive more of the cervical segmental veins than later. These, with the exception of the first, drain into the v. cardinalis posterior, but with the descent of the heart and great vessels, the cervical veins become tributaries of the anterior cardinal.


82 It is of interest to note that Davis (1910) has demonstrated open connections between the subcardinal veins and the portal system in early embryos of the pig, but these reach their maximum and are obliterated before the vena cava is formed.


83 Hoehstetter thus names the trunk passing from the liver to the heart and formed, as we have already seen, from parts of the hepatic, umbilical, and omphalomesenteric veins. It has been pointed out that some of the blood from the lower limbs and tail can stream through the sinusoidal vessels of the Wolffian body and join the vena cava, thus giving us a partial renal-portal system for the mesonephros of mammals. Yet in mammalian embryos we must grant Hochstetter's remarks that the characteristic renal-portal system of Sauropsida is only approached.



682 founded on a satisfactory series of human embryos, is still lacking. I shall accordingly content myself here with a brief presentation of the essential facts won from other mammalian embryos and of the probable history in man. This is the more justifiable also, since we possess many scattered observations, on such human material as has been at hand, by Hochstetter, Zumstein, and Kollmann, among others.


The exact manner in which the cardinal system is tapped by the hepatic was pointed out by F. T. Lewis (1902) and more recently by D. M. Davis (1910). The latter observer has shown that the capillaries on the ventral surface of the Wolffian body proliferate in a cephalic direction, fusing with capillaries which surround the oesophagus (peri-cesophageal plexus) and which course also on the

V. hepatica comm.



Lung

Cava mesenterii


Capillaries on the end of the v. subcardinalis

V. portse

Anastomoses between Anlage of the Anlage of the dorsal Aorta ventral pancreas pancreas

Anastomoses oetwei the umbilical veins

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

wall of the stomach. Thus the drainage territory of the subcardinal vein is extended headward. On the right side, beyond the anterior limit of the Wolffian body, this skirmish line of capillaries grows in the connective tissue of the caval mesentery which has also been invaded by hepatic capillaries in advance of liver cells. Soon hepatic and subcardinal capillaries meet and fuse, and for the first time a vascular path is offered from the right subcardinal to the common hepatic vein (Fig. 465). Inasmuch as both subcardinal and cardinal veins are in frequent connection, this new path diverts much of the blood stream of the lower posterior cardinal, which formerly went to Cuvier's duct, through this new channel. Thus in the posterior cardinal veins we may now be said to have two blood streams, for the current in the lower part of both veins turns ventrally into the upper right subcardinal vein by virtue of the great anastomoses between cardinals and sub


DEVELOPMENT OF THE VASCULAR SYSTEM. 683 cardinals, whereas in that part of the posterior cardinals above the level of the Wolffian bodies the blood goes upward to the ductus Cuvieri. This leads to a more or less complete separation of the two portions of the posterior cardinal vein. The upper portions of these veins are transformed into the system of the azygos and hemiazygos veins of the adult; the lower portions undergo still other changes. 84 For a while, although disturbed by the migration of the permanent kidneys, 85 they remain quite symmetrical, and so the vena cava appears double in the region below the great anastomosis above mentioned. 86 Eventually, however, only the lower segment of the right posterior cardinal persists to constitute the peripheral segment of the single adult vena cava inferior, for the left vein atrophies 87 in virtue of anastomoses between the two cardinals which enable the right channel to drain satisfactorily all the blood. The chief of these anastomoses (the transverse iliac vein) enables the blood from the left pelvic region, and the left limb to drain practically entirely into the right cardinal. In this way the transverse iliac vein constitutes the tenninal portion of the left common iliac, which has hence a morphological value different from the terminal part of the right v. iliacus communis. 88 Anastomoses also enable the left lumbar veins to be carried across the vertebral column to open into the right lower cardinal (cava), whereas the upper great anastomoses between the cardinals remains as the proximal part of the left adult renal vein. It is only necessary to add that the subcardinal veins below the level of the great transverse anastomoses atrophy, while that portion of the left vein above this level functions as the proximal part of the left adrenal vein. It hence goes into the renal vein (which represents in part the original great trans-anastomoses), rather than into the vena cava directly, as the right adrenal vein does. • The vena cava inferior, then, is a composite vessel, and is formed, from the liver downward, of parts of the following veins : right hepatic vein, connecting vein in the caval mesentery, right upper subcardinal vein, and right lower posterior cardinal.



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


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


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


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



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

V.c.



V.c.p


V. I. f.



. u.



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


usually so extreme as is the case, for instance, with the rabbit, where the right vein alone persists. In man, as is well known, the left trunk is only interrupted, for, while the lower portion joins 88 In all accounts hitherto given us, the upper portions of the original posterior cardinal veins have been described as entirely separated from their lower portions by the great deflection of the venous blood current due to the appearance of the inferior cava, and this "separation" occurs at such a level (e.g., the eighth thoracic segment, rabbit) that these upper portions of the posterior cardinals must be subsequently extended to the end of the thoracic region to constitute the a2ygos of the adult. They are, in fact, described as actually "growing down" secondarily. Hochstetter (1903, p. 604) comments on the conditions he found in a 15.5 human embryo, in which the adrenal glands destroyed the symmetry of the posterior

DEVELOPMENT OF THE VASCULAR SYSTEM.



685

the right vein (v. azygos) by means of one or more large cross anastomoses, its upper portion, the so-called v. hemiazygos accessoria, continues to Cuvier's duct. 90 Information on the exact details of the transformations effected in these venous channels in various mammals should be sought in the papers of Hochstetter, Zumstein, Lewis, Grosser, McClure, Gosset, Parker and Tozier, Van Pee, Beddard, Soulie and Bonne.



Plexus v. e. s.



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


6. THE DEVELOPMENT OF THE VEINS OF THE BODY WALL.


We have seen that in young embryos the body walls are drained into the umbilical vein by an extensive svstem of tribu


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



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


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


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


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



DEVELOPMENT OF THE VASCULAR SYSTEM.



687

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


7. TEE DEVELOPMENT OF THE VEINS OF THE EXTREMITY.


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

P. C. V

T. e. v,


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



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


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

688

V. fetnoralis superficial

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


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


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



DEVELOPMENT OF THE VASCULAR SYSTEM.



i;s!i

Ramus perforans v. mammaria? interna

V. thoraco epigastrica

nus perforans v. mammalia? interns


Rami perforantes v. mammaria? interna?

V. thoraco. epigastrica

exus venosus mammilla;

Ramus perforans v. mammaria internae

V. epigastrica superficialis

V'. femoralis superficialis externa

V. saphena magna \V. saphena parva — ^^_ (v. saphena accessoria) Vv. dorsalis penis cutanea? Fig. 473. — Body-wall veins of a human fetus 35 mm. long. (Mall No. 449,) The specimen was secured alive through the kindness of Dr. Thomas Cullen and injected through one of the aa. umbilicales.


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

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


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


Vol. II.— 44

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

VJ,ing-fac

V.Hng-fac.



W^—V.card.ant.



V.card.towu.



Y.scl.d. \ %-V.cardposi


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


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


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


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






DEVELOPMENT OF THE VASCULAR SYSTEM.



691


W^SSk~ '"card.ant.



Kcard.com.



Vcard.post.



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



'M-Y.an.dext.


•Sty '-an. sin. =9fij V.mam. int.



Yth-ep.


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



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


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


Y. jugulai. int. f -.



V. jugularis ext.



V. jugulo-cephaliea

Anastomoses between tne \ v. anonvms

V. jugulocephalica

/



V. cepha lica

V*. cephalica

V. brachialis

V. brachialis

V. basilica


r \


V. basilica

Y. thoraco-epigastrica

Y. thoraco-epigastrica

Fig. 47S. — Reconstruction of the relations of the great veins of the arms and neck in a human embryo 20 mm. long. (Mall collection, No. 349.) radial side of the upper arm (Figs. 476, 477), and in an embryo of 22.8 mm. Lewis has shown that the cephalic vein now joins the external jugular, an arrangement which is true for the embryo figured in Fig. 478, but in which there is also now present a connection between the cephalic and the subclavian veins which is to function as the definitive proximal ending of the cephalic vein in man. This earlier drainage channel of the cephalic into the external jugular vein may persist (jiigulocephalic rein), as has been noted for many years in descriptive human anatomy.


The cephalic vein at the stage last mentioned has become the chief superficial vein of the arm, for, with the breaking up of the

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


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



DEVELOPMENT OE THE VASCULAR SYSTEM.



693

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

Jg£- V. cephaiica


,Vv. intercapitulares V. mediana antibrachii

V. basilica

I' [G8. 479 and Iso. — The superficial veins of the right arm in a human fetus 35 mm. long. From an injection. (The specimen is the same as that shown in Fig. 473.) of the arm veins in an embryo 35 mm. long shows thai even at this stage there are not yet formed the many connections between basilic and cephalic veins which constitute the well-known venous plexus of the dorsum mani and the forearm. It is thus possible to state that the great subcutaneous venous plexuses of the extremity are not partial remains of a primary embryonic more

694 extensive plexus, for the only primary plexus existing here is again a general capillary mesh, and the larger venous connections which characterize the adult are clearly secondary formations. In the arm figured, one may see the earliest veins of the volar surface of the forearm, and, especially clearly, the method of formation of the v. mediana antibrachii through the enlargement of parts of the general capillary mesh (Fig. 480).


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


Fig. 481.



Fig. 482.



Fig. 481. — The fibular border vein in a human embryo 15.5 mm. long. (Mall collection, No. 390.) (After a sketch kindly placed at my disposal by Mr. Max Broedel.) Fig. 482. — The fibular border vein in an injected human embryo 21 mm. long. (Mall collection, No. 460.) The vein is seen to drain the dorsum of the foot by a distinct venous arch; the proximal portion of the original border vein can be recognized.


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

DEVELOPMENT OF THE VASCULAR SYSTEM.



695

the v. femoralis, which has developed along the permanent artery (a. femoralis) of the limb (the v. ischiadica in the adult being important only as a collateral path for the blood). The early


V. saphena parva

Fig. 4S3. — The fibular border vein (v. saphena parva) in a human embryo 23 mm. long (Mall No. 462) at a time when toes and heel are clearly evident.



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


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

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

V. cava inf.



V. epigastrica Vena femoralis superficialis superficialis externa

V. saphena magna

V. saphena parva

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

V. femoralis superficialis externa


V. saphena magna

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

length, I have found this connection a constant feature, practically all the blood of the lower leg vein {v. saphena parva) going

DEVELOPMENT OF THE VASCULAR SYSTEM.



697

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


V. .-aphena accessoria

V. saphena magna

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

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



698 HUMAN EMBRYOLOGY.


In the development of the leg, the proximal portion of the extremity is for a while buried, as it were, in the tissues of the embryo, and only in embryos of some 20 mm. in length, and in those older than this, can we speak of a cutaneous surface belonging to the inner side of the thigh. Consequently the saphena parva is in the position to drain the early venules which come from the neighborhood of the perineum and buttock (if we may yet speak of the latter), as Fig. 481 will show. With the "pushing out" of the thigh, this is no longer possible, 9s for the proximal end of the saphena parva is carried out with the knee, and the saphena magna is now the direct and natural channel for this blood. In embryos measuring 50 mm. in length the vessels draining the back of the buttocks into the saphena magna constitute a large and prominent system (Fig. 484).


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


General.


Aeby, C. : Der Bau des menschlichen Korpers. Leipzig 186S.


Arnold, J. : Experimentelle Untersuchungen iiber die Entwicklung der Blutkapil laren. Virchow's Arch. Bd. 53, S. 70. 1871. Backman, G. : Ueber Inselbildung im Gefasssvstera. Anat. Hefte. Bd. 38. Heft 114. S. 1. 1909. Balfour, F. M. : Comparative Embryology. London 1885.


Billroth, T. : Untersuchungen iiber die Entwicklung der Blutgef asse. Berlin 1856. Bobritzky: Entwicklung der Kapillargefasse. Centralbl. f. med. Wiss. Bd. 23.


1885. Broman, J. : Beschreibung eines menschlichen Embryo. Morph. Arb. Bd. 5. 1S96. Bryce, T. H. : "Embryology" in Quain's Anatomy, 11th Edition. London 1908. Clarke, E. R. : Observations on Living Growing Lymphatics in the Tail of the Frog Larva. Anat. Record. Vol. 3, No. 4. 1909. Drasch, O. : Die Bildung der Somatopleura und der Gefasse beim Hiihnchen. Anat.


Anz. Bd. 9. 1894. Duval: Etudes stir Fembryologie des Cheiropteres. Journ. de l'Anat. et de la Phvs.


1897. Elze, C. : Beschreibung eines menschlichen Embryo von ea. 7mm. grosster Lange usw. Anat. Hefte. Bd. 35. Hefte 106. S. 411. 1907.


"* Except, of course, in those eases in which, as in Fig. 4S6, the saphena parva continues up the inner side of the thigh.


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



DEVELOPMENT OF THE VASCULAR SYSTEM. 699 Eternod, A. C. F. : Communication sur un oeuf humain avec embryon excessive ment jeune. Xleme Congres medical de Rome. Section d'Anatomie. 1894. Sur un oeuf humain de 16mm, 3 avec embryon de 2,11 mm, uterus et annexes.


Actes de la Soc. helvet. des sc. natur. p. 164-169. 1896. Premiers stades de la circulation sanguine dans l'ceuf et l'embryon humain. Anat.


Anz. Bd. 15, S. 181. 1898. II y a un canal notochordal dans l'embryon humain. Anat. Anz. Bd. 16, S.


131-143. 1899. L'anse veineuse vitelline des Primates (Homme et Quadrumanes). C. R. de P Association des Anat. 4eme Sess. p. 103-110. Montpellier 1902. Zwei menschliche Embryonen von 1.3 mm und 2.11 mm Lange usw. Gynaeco log-ica helvetica. 4. Jahrg. S. 21-23. 1904. L'ceuf humain. Memoire public a l'occasion du Jubile de l'Universite de Geneve.


Geneve 1909. Evans, H. M. : On the Development of the Aorta, Cardinal and Umbilical Veins, and the other Blood-vessels of Vertebrate Embryos from Capillaries. Anat.


Record. Vol. 3, p. 498-518. 1909. Fleischmann: Embryologische Untersuchungen. Heft 1 u. 2. 1889-1891. Frassi, L. : Ueber ein junges menschliches Ei in situ. Arch, f . mikr. Anat. Bd. 70, S. 492. 1907. Weitere Ergebnisse des Studiums eines jungen menschlichen Eies in situ. Arch.


f. mikr. Anat. Bd. 71, S. 667-694. 1908. Gerard, G. : Les canaux anastomotiques arterio-veneux chez Fhomme et chez les singes. Arch, des Sci. Medicales. T. 1 und Les anastomoses directes entre les arteres et les veines. Poid. T. 3. 1896. Goette, A. : Entwicklungsgeschichte der Unke. Leipzig 1875. Golubew: Beitr. zur Kenntnis des Baues und der Entwicklung der kapillaren Gefasse. Arch. f. mikr. Anat. Bd. 5, S. 85. 1869. Grosser, O. : Zur Anatomie und Entwicklung des Gefasssystems der Chiropteren.


Anat. Hefte. Bd. 17. 1901. Ueber arterio-venose Anastomosen an den Extremitatenenden beim Menschen und den krallentragenden Saugetieren. Arch. f. mikr. Anat. Bd. 60, S.


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Vol. 23. 1883. Hess, W. : Eine mechanisch bedingte Gesetzmassigkeit im Bau des Blutge fasssystems. Arch. f. Entwicklungsmechanik. Bd. 16. 1903. His, W. : Anatomie menschlicher Embryonen. Heft 1~3. Leipzig 1880-1885.


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DEVELOPMENT OF THE VASCULAR SYSTEM. 701 Robixsox : Observations upon the Development of the Segmentation Cavity, etc.


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Jour, of Anat. and Phys. Vol. 16. 1907. Turstig, J. : Untersuchungen fiber die Entwicklung der primitiven Aorten. Sckrift., berausgegeben v. d. Xaturf.-Ges. bei d. Univ. Dorpat. Bd. 1. Dorpat 1SS4. Van Beimelen, E. and Julix. C. : Recherches sur la formation des annexes fcetales chez le mammiferes. Arch. d. Biol. T. 5. 1SS4. Vastarixi, C. G. : Le anastomosi artero-venose nell' uomo e nei mammif eri. Studio anatomo-Lstologico. p. 176. Napoli 1902. Vialleton, L. : Developpement des aortes chez l'embiyon de poulet. Journ. de l'Anat. et de la Phys. T. 28, p. 1. 1892. Vosmaer, G. C. J. : On the Retrograde Development of the Blood-vessels in the Omentum of the Rabbit. Verslag v. d. Gew. Vergad. d. Mis. Naturk. Afd.


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Baader, A. : Ueber die Varietaten der Armarterien des Menschen und ihre morpho logisehe Bedeutung. Inaug.-Diss. Bern 1866. Baer, K. E. v.: Ueber die Kieinen und Kiemengefasse in den Embryonen der Wirbeltiere. Meckel's Arch. 1827. Des branches et des vaisseaux branchiaux dans les embryons des animaux vertebres. Annal. des Sciences Naturalist. Tome 15. 1828. Barpi, U. : Intorno ai rami minori del' aorta abdOminale ed all' irrigazione arteriosa del ganglio semilunare, del plesso solare e delle capsule surrenali negli equini, nei carnivori e nei roditore domestici. Arch. Ital. Anat. e di Embriol. Vol.


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1909. Castellani, L. : Osservazione sullo sviluppo della circolazione sanguigna del rene umano. Ricerche fatte nei Labor. Anat. normale di R. Univ. di Roma et in altri Labor. Vol. 12. Fasc. 4, p. 225-252. 1907. Clark, John G. : The Origin and Degeneration of the Blood-vessels of the Human Ovary. Johns Hopkins Hospital Reports. Vol. 9. 1900. Dedekind, F. : Beitrage zur Entwicklungsgeschichte der Augengefasse des Menschen. Anat. Hefte. Bd. 38. Heft 114. S. 1. 1908. Dohrn, A. : Studien zur Urgeschichte das Wirbeltierkorpers. XV. Mitt. a. d. Zool.


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Fasc. 4. 1907. Ernst, P. : Unpaariger Ursprung der Intercostal- und Lumbalarterien aus der aorta. Zeitschr. f. Morph. u. Anthrop. Bd. 1, S. 495. 1899. Evans, H. M. : On an Instance of Two Subclavian Arteries in the Early Arm Bud of Man. Anat. Record. Vol. 2. 1908. On the Earliest Blood-vessels in the Anterior Limb Buds of Birds and their Relation to the Primary Subclavian Artery. Amer. Journ. of Anat. Vol 9.


1909. Fedorow, V. : Ueber die Entwicklung der Lungenvene. Anat. Hefte. Bd. 40, S.


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DEVELOPMENT OF THE VASCULAR SYSTEM. 703 Felix, W. : Zur Entwicklungsgeschichte der Rumpfarterien des menschlichen Embryo. Morph. Jahrb. Bd. 41. Heft 4. S. 577. 1910. Fere, C. : Vaisseaux omphalo-rnesenteriques. Bull. Soe. Anat. Paris 1878. Fetzer : Ueber ein dureh Operation gewonnenes menschlicbes Ei, das in seiner Entwicklung etwa dem Peter'schen Ei entspricbt. Verh. Anat. Ges. Erg. Heft des Anat. Anz. Bd. 37, S. 116-126. 1910. Flint, J. M. : Tbe Blood-vessels, Angiogenesis, Organogenesis, Reticulum, and Histology of the Adrenal. Jobns Hopkins Hospital Reports. Vol. 9. 1900. The Angiology* Angiogenesis, and Organogenesis of the Submaxillary Gland.


Amer. Journ. of Anat. Vol. 2, p. 417-444. 1903. The Development of the Lungs. Amer. Journ. of Anat. Vol. 6, p. 1-137. 1906. Fransen, J. W. P. : Le systeme vasculaire abdominal et pelvien des primates.


Petrus Camper. Deel 4. S. 215. 1907. Frederic, J. : Beitrag zur Anatomie und Entwicklungsgeschichte der Aste der aorta descendens beim Menschen. Schwalbes Morph. Arb. Bd. 7. 1897 auch Med. Diss. Strasburg 1898. Fuchs, H. : Zur Entwicklungsgeschichte des Wirbeltierauges. Anat. Hef te. Bd.


28. Heft 83. Wiesbaden 1905. Goppert, E. : Die Beurteilung der Arterienvarietaten der oberen Gliedmasse bei den Saugetieren und beim Menschen auf entwicklungsgesckichtlicher und vergleichend anatomischer Grundlage. 22 Fig. Ergebn. d. Anat. u. Ent wicklungsgesch. Bd. 14. 1905. Variabilitat im embryonalen Arteriensystem. Verhandlungen der anat. Ge sellschaft. 22. Versammlung. Erg.-Heft z. Anat. Anz. Bd. 32, S. 94.


1908. Ueber Riickbildung und Ersatz der arteria brachialis bei Echidna. Morph.


Jahrb. Bd. 33. 1909. Ueber die Entwicklung von Varietaten im Arteriensystem. Morph. Jahrb. Bd.


40. Heft 2 u. 3, S. 268^10. 1909. Grape, E. : Beitrage zur Entwicklung der Urniere und ihrer Gefasse beim Hiihn chen. Arch. f. mikr. Anat. Bd. 67. 1905. Grosser, O. : Zur Frage der segmentalen Gef assversorgung der Haut beim Menschen. Morph. Jahrb. Bd. 33, S. 555-561. 1905. Der Nerv des funften Visceralbogens beim Menschen. Anat. Anz. Bd. 37, S. 333-336. 1910 1 . Zur Kenntnis des ultimobranchialen Korpers beim Menschen. Anat. Anz.


Bd. 37, S. 337-342. 1910 2 . Hammar, J. A. : Ein beachtenswerter Fall von Halskiemenfistel. Ziegler's Beitr. z.


path. Anat. Bd. 36. 1904. Henneberg, B. : Verhalten der Umbilicalarterien bei den Embryonen von Ratte und Maus. Anat. Anz. Bd. IS, S. 321-324. 1900. Ueber die Anatomie und Physiologie der Umbilicalgefasse des Menschen. 34 Ber. Oberhess. Ges. f. Nat. u. Heilk. Med. Abt. Bd. 2, S. 11. 1901. Hepburn, D. : Halichoerus grypus, the Gray Seal. Journ. of Anat. and Phys. Vol.


30. N. S. Vol. 10, p. 498. 1896. ' Hill, E. C. : First Appearance of the Renal Artery. Johns Hopkins Hosp. Bui.


Vol. 16, p. 60. 1905. Hirsch, C. : Ueber die Entwicklung der Hornhautgefasse. Verh. d. Ges. deutsch.


Naturf . u. Arzte in Karlsbad 1902. Bd. 2. Heft 2. S. 382-383. (Erschien 1903). His, W. : Zur Bildungsgeschichte der Lungen beim menschlichen Embryo. Arch.


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704 HUMAN EMBRYOLOGY.


Hochstetter, F. : Ueber die Entwicklung der a. vertebralis beiru Kaninchen, nebst Beinerkungen iiber die Entstehung der ansa Vieussenii. Morph. Jahrb. Bd 16, S. 572-586. Taf. 21. -1890. Ueber den Ursprung der arteria subclavia der Vdgel. Morph. Jahrb. Bd. 16.


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Janosik, J. : Le developpenient des vaisseaux sanguins et des nerfs du membre anterieur cbez l'bomme et cbez quelques autres animaux. Arch, bohemes de Med. T. 4. 1891. Jeidell, H. : A Note on the Source and Character of the Early Blood-vessels of the Kidney. Anat. Record. Vol. 5. No. 2. 1911. Kadyi, H. : Ueber die Blutgefiisse des menschlichen Ruckenmarkes. Lemberg 1889. Kolster, R. : Studien liber die Niereno-ef asse. Zeitsehr. f . Morphol. u. Antbrop.


Bd. 4, S. 179. 1901. Krause, W. : Varietaten des Aortensystems und Varietaten der Korpervenen. Henle's Handbuch der syst. Anat. des Menschen. Bd. 3 : Gef asslehre. Braunschweig 1876. Leboucq : In der Disc, zu Zuekerkandl's Vortrag. Verb. d. anat. Gesellschaf t.


Erg.-Heft z. Anat. Anz. Bd. 8. 1893. Lehman, H. : On the Embryonic History of the Aortic Arches in Mammals. Anat. Anz. Bd. 26, S. 406^24. 1905. On the Embryonic Histoiy of the Aortic Arches in Mammals. Zool. Jahrb. Abt. f. Anat. Bd. 22, S. 387^34. 1905. Levi, G. : Morphologia delle arterie iliache. Arch. ital. di Anat. e di Embriologia.


Vol. 1. 1902. Lewis, F. T. : The Intra-Embryonic Blood-vessels of Rabbits from S l A to 13 days. Amer. Journ. of Anat. Vol. 3, p. 12-13. (Proc. Amer. Ass. Anat.) 1904. The Fifth and Sixth Aortic Arches and the Related Pharyngeal Pouches in the Rabbit and Pig. Anat. Anz. Bd. 28, p. 506. 1906. Locy, W. A. : The Fifth and Sixth Aortic Arches in Chick Embryos, with Comments on the Condition of the Same Vessels in other Vertebrates. Anat. Anz. Bd. 29. 1906. The Fifth and Sixth Aortic Arches in Birds and Mammals. Advance Print Proceedings of Seventh International Zoological Congress. Cambridge 1909. Luna, E. : Zur Morphogenese der unteren Zwerchfellarterien beim Menschen.


Arch. f. Anat. u. Phys. Anat. Abt. 1908. Macalister, A. : Multiple Renal Arteries. Journ. of Anat. and Phys. Vol. 17, p.


250. 1883. MacCallum, J. B. : Notes on the "Wormian Bodv of higher Mammals. Amer. Journ. of Anat. Vol. 1. 1902.



DEVELOPMENT OF THE VASCULAR SYSTEM. 705 Mall, F. P. : Development of tbe Human Coslom. Journ. of Morphol. Vol. 12, p.


395. 1897. Development Internal Mammary and Deep Epigastric Arteries in Man. Johns Hopkins Hospital Bulletin. 1898. On the Development of the Blood-vessels of the Brain in the Human Embryo.


Amer. Journ. of Anat. Vol. 1, p. 1. 1904. A Study of the Structural Unit of the Liver. Amer. Journ. of Anat. Vol. 5, p. 227. 1906. Manchot, C. : Die Hautarterien des mensehlichen Korpers. Leipzig. 1889. Manno, A. : Sur un cas interessant de "arteria saphena magna" chez l'homme.


Bibliogr. Anat. T. 14. Paris 1905. Martin, H. : Recherches anatomiques et embryologiques sur les arteres coronaires du coeur chez les vertebres. These Med. Paris 1894. Note sur le permier developpement des arteres coronaires cardiaques chez l'embryon du lapin. C. R. Soc. Biol. Ser. 9. T. 6. p. 83-85. 1894. Muller, E. : Beitrage zur Morphologie des Gef asssystems. I. Die Armarterien des Mensehen. Anat. Hefte. 1903. II. Die Armarterien der Saugetiere.


Anat. Hefte. 1904. III. Zur Kenntnis der Fliigelarterien der Pinguine.


Anat. Hefte. 1908. Parsons, F. G. : On the Arrangement of the Branches of the Mammalian Aortic Arch. Journ. of Anat. and Phys. Vol. 36, p. 389-399. London 1902. Pensa, A. : Studio sulla morph. e. s. sviluppo della a. intercost supr. Ric. f atte nel Lab. di Anat. umana normale della R. Univ. di. Roma etc. Vol. 2. Roma 1905. Osservazioni sulla moiphologia e sullo sviluppo della arteria pulmonalis nell'uomo. Boll, della Soc. Med. Chir. di Pavia, Communicazione fatta nella seduta del 8 Aprile 1910. Pavia 1910. Peter, K. : Mitteilungen zur Entwicklungsgeschichte der Eideehse. Arch, f . mikr.


Anat. Bd. 57. 1901. Ppeipfer, B.: Zur Kenntnis des histologisehen Baues und der Riickbildung der Nabelgefasse und des ductus Botalli. Virchow's Arch. Bd. 167, S. 210-231.


1902. Picchini, L. : Sviluppo dell' arteria pulmonare dell' aorta. II Morgagni. Vol. 33, p. 779-783. Napoli 1891. Popopf, D. : Die Dottersackgefasse des Huhnes. Wiesbaden. 1894. Popowsky: Ueberbleibsel der arteria saphena beim Mensehen. Anat. Anz. Bd. 17.


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Arch. f. mikr. Anat. Bd. 69. 1907. Rathke, H. : Ueber die Entwicklung der Arterien, welche bei den Saugetieren von den Bogen der aorta ausgehen. Mulleins Arch. f. Anat. u. Phys. S. 276.


1843. Ravn, E. : Uber die arteria omphalo-mesenterica der Ratten und Mause. Anat. Anz.


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25, S. 321. 1904.


Vol. II.— 45

706 HUMAN EMBRYOLOGY.


Salensky, W. : Beitriige zur Entwicklungsgeschiehte der knorpeligen Gehorknochel chen bei Saugetieren. Morpk. Jahrb. Bd. 6. 1880. Salvi, G. : Arteriae superfieiales. Monitore Zoologico Italiano. T. 10. 1899. Schultze, 0. : Zur Entwicklungsgeschiehte des Gefasssystenis im Siiugetierauge.


Festschr. f. Kolliker. Leipzig 1892. Schwalbe, E. : Beitrag zur Kenntnis der Arterien- Varietaten des menschlichen Armes. Schwalbe's Morph. Arbeiten. Bd. 8. 1898. Semon, R. : Studieu iiber den Bauplan des UrogenitaLsy steins der Wirbeltiere.


Jenaische Zeitschr. f. Nat. Bd. 26. 1891. Soulie et Bonne : Contribution a Petude de l'appareil branchial et des arcs aortiques chez les mammiferes. Journ. de l'Anat. et de la Phys. Vol.


44. 1908. Sterzi, G. : Die Blutgef asse des Riickenmarks. Anat. Hefte. Abt. 1. Bd. 24, S. 3^364. Taf. 1-4. 1904. Tandler, J. : Zur Entwicklungsgeschiehte der Kopf arterien bei den Mammalia.


Morph. Jahrb. Bd. 30, S. 275-373. 1902. Zur Entwicklungsgeschiehte der menschlichen Daimarterien. Anat. Hefte.


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London 1892. Tonge, M. : Observations on the Development of the Semilunar Valves of the Aorta and Pulmonary Artery of the Heart of the Chick. Phil. Trans. 1869. Tonkoff, W. : Die Arterien der Intervertebralganglien und der Cerebrospinalnerven des Mensehen. Internat. Monat. f. Anat. u. Phys. Bd. 15. 1898. Die nervenbegleitenden Gefassnetze beim Embryo und die arteriae nutriciae nervorum beim Erwachsenen. Anat. Anz. Bd. 30. 1907. Vebsari, R. : Morfologia dei vasi sanguigni ai-teriosi dell' ochio dell' uomo e di altri mammiferi. Rieerche fatte nel Lab. d. Anat. umana norm, della R.


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DEVELOPMENT OF THE VASCULAR SYSTEM. 707 Observations on the Development and Morphology of the Tail. Brit. Med. Joum. Vol. 2, p. 1384-1391. 1904. Young, A. H., and Thompson, P.: Abnormalities of the Renal Arteries, with Remarks on their Development and Morphology. Joum. of Anat. and Phys. Vol. 38. 1903. Zagorsky: Mem. de l'acad. des Seienc. de St. Petersbourg. Vol. 1, p. 326. 1809. Zimmekmaxx, W. : Ueber die Kiemenarterienbogen des Menschen. Verb. d. 10. internat. med. Kongr. Berlin. Bd. 2. Abt. 1. 1S90. Ueber emen zwischen Aorten und Pnlmonalbogen gelegenea Kiemenarterienbogen beim Kaninchen. Anat. Anz. Bd. 4, S. 720. 18S9. Zuckerkaxdl : Ueber die Entstehung der Vorderarnigefasse beim Kaninchen und bei der Katze. Verb. Anat. Ges. Erg.-Heft z. Anat. Anz. Bd. 8, S. 126-129. 1893. Zur Anatomie und Entwieklungsgesehichte der Arterien des Vorderarmes.


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Veins.


Anikiew. A.: Zur Frage iiber die Entwicklung der vena anonyma sinistra. Anat.


Anz. Bd. 34, S. 24. 1909. Bardeleben, K. vox: Die Hauptvene des Ai'mes, vena capitalis braehii. (Ueber die Entwicklung der Extremitatenvenen des Menschen.) Jenaische Zeitschr.


f. Naturw. Bd. 14. 1879. Benigxi, E. : Persistenza della vena ombilicale nelF adulto. Gazz. Ospidali. Anno 25. N. 85, p. 894-895. Bonnot and Seevers: On the Structure of a Human Embryo Eleven Millimetres in Length. Anat. Anz. Bd. 29, S. 452-459. 1906. Broman, I. : Ueber die existenz eines bisher unbekannten Kreislaufes im embi'yona len Magen. Anat. Anz. Bd. 23, S. 390-391. 1903. Rtrow: Beitrag zur Gefiisslehre des Fetus. Mfdlcr's Arch. S. 44. 1838. Davis. D. M. : Studies on the Chief Veins in Early Pig Embryos and the Origin of the Vena Cava Inferior. Amer. Joum. of Anat. Vol. 10, p. 161-472. 1910.



708 HUMAN EMBRYOLOGY.


Dexter, F. : On the Vitelline Vein of the Cat. Anier. Journ. of Anat. Vol. 1, p.


261-267. 1902. Duval, M. : Apropos des veines ombilieales. Bull. Soe. Biol. Paris 1889. Gosset, A. : Contribution a l'etude du developpement de la veine cave inf erieure et des veines renales. Bull. Soe. Anat. Annee 73. Ser. 5. Vol. 12. Paris 1898. Grosser, 0., and Brezina, E. : Ueher die Entwieklung der Venen des Kopfes und des Halses bei Reptilien. Morph. Jahrb. Bd. 23. 1895. Zur Anatomie und Entwicklungsgeschichte des Gefasssystems der Chiropteren.


Anat. Hefte. Bd. 17. Heft 55. S. 131. 1901. Die Elemente des Kopfvenensystems der Wirbeltiere. Verb. d. Anat. Ges. Erg.-Heft z. Anat. Anz. Bd. 30, S. 179-192. 1907. Hochstetter, F. : Ueber die Bildung der hinteren Hohlvene bei den Saugetieren. Anat. Anz. Bd. 2. 1887. Ueber den Einfluss der Entwieklung der bleibenden Niere auf die Lage des Urnierenabsehnittes der hinteren Kardinalvenen. Anat. Anz. Bd. 3. 1888. Ueber die Entwieklung der Extremitatenvenen bei den Amnioten. Morph.


Jahrb. Bd. 17. 1891. Beitrage zur Entwicklungsgeschichte des Yenensystems der Amnioten. Sanger.


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Nat, Hist. Vol. 28 and Science N. S. Vol. 7. 1898.^ Parker, G. H. and Tozier, C. H. : The Thoracic Derivatives of the Postcardinal Veins in Swine. Bull. Mus. Comp. Zool. Harvard 1898.



DEVELOPMENT OF THE VASCULAR SYSTEM. 709 Pee, P. van: Note sur le developpement du systeme veineux du foie chez les em bryons de lapin. Journ. de l'anat. et de la phys. Vol. 35. Paris 1899. Piersol, G. A. : Human Anatomy. Philadelphia 1907. Popoff, D. : Die Dottersackgef asse des Huhnes. Wiesbaden 1894. Rex, H. : Beitrage zur Morphologie der Saugerleber. Morph. Jahrb. Bd. 14, S.


517-617. 188S. Salvi : Sopra lo sviluppo delle meningi cerebrali. Pisa 1897. Salzer, H. : Ueber die Entwieklung der Kopfvenen des Meerschweinchens. Morph.


Jahrb. Bd. 22. 1895. Schawlowski, I. : Zur Morphologie der Venen der oberen Extremitat und des Halses. Dokt.-Diss. St. Petersburg 1S91. (Compare Stieda, ref. in Ergebn. d. Anat. u. Entw. von Merkel u. Bonnet. Bd. 3, S. 380. 1894.) Smith, W. H. : On the Development of the Superficial Veins of the Body Wall in the Pig. Amer. Journ. of Anat. Vol. 9. July 1909. Soulie, A., et Bonne, C. : Reeherehes sur le developpement du systeme veineux chez la taupe. Journ. de l'anat. et de la phys. Vol. 41, No. 1, p. 1-39. 1905. Tandler, J. : Die Entwieklung der Lagebeziehung zwischen n. accessorius und v.


jugularis interna beim Menschen. Anat. Anz. Bd. 31, S. 473-480. 1907. Thompson, P. : A Note on the Development of the Septum Transversum and the Liver. Journ. of Anat. and Phys. Vol. 42, p. 170-175. 190S. Wertheimer, E. : Reeherehes sur la veine ombilicale. Journ. de l'anat. et de la phys. Vol. 22. Paris 1886. Williams, L. W. : The Somites of the Chick. Amer. Journ. of Anat. Vol. 11. No.


1, p. 55. 1910. Woodland, W. : A Suggestion concerning the Origin and Significance of the Renal-Portal System, with an Appendix relating to the Production of Subabdominal Veins. Proc. Zool. Soc. Lond., p. 887-901. 1906. Zumstein, J. : Zur Anatomie und Entwieklung des Venensystems des Menschen.


Anat. Hefte. Bd. 6. 1896. Zur Entwieklung des Venensvstems beim Meerschweinchen. Anat. Hefte. Bd.


8. 1897. Ueber die Entwieklung der vena cava inferior bei dem Maulwurfe und bei den Kanincheu. Anat. Hefte. Bd. 10. 189S.


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

XVIII. Development of Blood, Vascular System and Spleen: Introduction | Origin of the Angioblast and Development of the Blood | Development of the Heart | The Development of the Vascular System | General | Special Development of the Blood-vessels | Origin of the Blood-vascular System | Blood-vascular System in Series of Human Embryos | Arteries | Veins | Development of the Lymphatic System | Development of the Spleen
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   Manual of Human Embryology II 1912: Nervous System | Chromaffin Organs and Suprarenal Bodies | Sense-Organs | Digestive Tract and Respiration | Vascular System | Urinogenital Organs | Figures 2 | Manual of Human Embryology 1 | Figures 1 | Manual of Human Embryology 2 | Figures 2 | Franz Keibel | Franklin Mall | Embryology History