Paper - Development of the internal mammary and deep epigastric arteries in man (1898)

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Mall FP. Development of the internal mammary and deep epigastric arteries in man. (1898) Johns Hopkins Hospital Bulletin 9: 232.

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Development of the Internal Mammary and Deep Epigastric Arteries in Man

Franklin Mall (1911)
Franklin Mall

By Franklin P. Mall.

From the Anatomical Laboratory of the Johns Hopkins University.


The great importance of the fact that the main arteries of the vertebrates arise directly from the aortic arches has been shown repeatedly in ontogenetic and phylogenetic studies. Furthermore, it gives us a scientific basis for the explanation of the numerous variations which may occur while this simple system of arteries is being transformed into the complex system as found, for instance, in man.

While the modification of the aortic arches is taking place, certain arteries become larger, others disappear, while in others tlie direction of the circulation is reversed. The laws governing these changes have been discussed extensively by Thoma in his numerous communications. It is the law of use and disuse expressed in this instance by rapidity. For a given vessel at a given time in its development there is a certain rapidity of circulation through it at which it ceases to grow. If the rapidity of the circulation is increased the vessel becomes larger ; if it is diminished the vessel becomes smaller ; if the circulation comes to a standstill the vessel disappears altogether. This law is constantly at work throughout development in the grown animal and in all pathological changes. It does not appear to govern the firstgrowth of the capillaries but itgoverns the growth of the vessels after the circulation in them is once started.

Any one who has studied the growth of the blood-vessels extensively in living animals as well as in fixed preparations is well aware of the fact that blood-vessels are constantly being formed and destroyed. This process is so extensive that at almost any stage of the development of an animal we may safely say that more blood-vessels have disappeared than are present at that time.

With the above ideas clearly in view, I have studied the extension of the blood-vessels into the body- walls of the embryo to see whether or not some secondary system, regular like the aortic arches, appears to be subsequently converted into the main arteries of the body- walls and the extremities. That the vertebral artery is formed by the union of a number of branches from the descending aorta has been shown by His,* by Froriepf and by Hochstetter.J These branches are the segmental arteries from the aorta while it is still in the branchial region. The aorta soon shifts away from the branchial region with the bending of the head and the development of the neck. While this is taking place the segmental arteries unite at their distal ends to form the vertebral artery while the communicating branches are gradually broken off as shown in Fig. 1, V, from a human embryo of the fourth week. This process continues down to the seventh cervical segmental artery, where it ceases. At this point the subclavian artery arises, Fig. 1, S, as shown by Hochstetter. From now on for a few segments the process is very diflBcult to follow, but further on throughout the thoracic region of the embryo the process is simple. This is easily accounted for by the perfect segmental arrangement of this portion of the body throughout its development.

There are, however, two other sets of segmental arteries in the thoracic region of the body which appear before this set is formed and gives rise to the arteries of the body-walls. The first set is already well developed in embryos at the end of the second week.§ They arise from the aorta and pass immediately to the umbilical vesicle, there to break up into a plexus which is collected by the omphalo-niesenteric veins. Soon these arteries disappear and the omphalo-mesenteric artery takes their place. These vessels are of course on the mesial side of the coelom.

Hi8(W.) Anat. mensch. Embryonen. III. Zuf Geschiehte der Organe, Leipz., 1885.

fFroriep (A.) Arch. f. Anat. u. Physiol., Anat. Ablh., Leipz., 1SS6, S. 69-1.50.

t Hochstetter (F.) Morphol. Jahrb., Leipz., Bd. xvi, 1890.

? Mall (F. P.) J. Morphol., Bost., Vol. xii, 1896-7, Fig. 16.

Before this first system has disappeared, and before the permanent intercostal vessels have appeared the second set of segmental arteries arises from the descending aorta, passes on the lateral side of the ccelom into the menibrana reuniens, as is indicated to us by a figure given by von Kiilliker,* as well as by the description of His.f Von Kiilliker pictures a cow's embryo with the whole membrana reuniens filled with a minute plexus of veins which radiate from the myotomes towards the umbilical cord, while His describes this same region in the human embryo as filled with branches of the umbilical vein which empty into the sinus reuniens above, and into the umbilical vein below. According to His's description they arise when the communication between the umbilical veins and the sinus reuniens is severed. Although the picture given by von Kolliker does not correspond with His's description it does not contradict it, nor is it peculiar to the cow's embryo. I have in my collection a well-preserved human embryo (No. LXXVI), in which the membrana reuniens is filled with a plexus of veins much like that in the cow's embryo. The specimen was taken from the uterus seven hours after the death of the woman, and without opening, the ovum was hardened in absolute alcohol. All the vessels down to the capillaries are filled with blood, thus making it an excellent specimen for the study of the blood-Tessels. It represents a stage somewhat more advanced than the one pictured by von Kiilliker, as the plexus of veins does not cover the whole membrana reuniens. The ventral wall over the heart near the liver contains no vessels, while the membrana reuniens covering the upper end of the heart is filled with a plexus of vessels which communicate with the capillaries of the mandibular arch. ., There is an extensive plexus through the arm and lateral body walls which extends through the menibrana reuniens covering the liver, and finally encircles the cord and communicates with the umbilical veins.

Fig. 1. — Arterial system of a humau embryo four weeks old (No. II). Enlarged 10 times. F, vertebral artery; P, pulmonary artery ; C, creliac axis; S, subclavian artery ; 4, fourth dorsal seijmeutal artery.

von Kolliker (A.) Grundrisa der Eutwicklungsgeschichte des MenschenundderhiJherenThiere. 8°. Leipzig, 1880. S.103, Fig. 85.

fHisCW.) Anatomie menschlicher Embryonen. Ill, Zur Geschichte der Organe. Leipzig, 1885, 8°. S. 206, also Fig. 130,

The specimen just described is about 22 days old and, although I have six other good embryos between 14 and 28 days old, I find no such plexus in the membrana reuniens, although in all but one of them (14 days) the arm shows a rich plexus of capillaries filled with blood. In stages older than four weeks I find no blood-vessels in the membrana reuniens with the exception of that portion encircling the cord, where there is a rich network of veins. Although I have a number of excellent specimens of five or six weeks, the membrana reuniens over the heart and liver contains no blood-vessels until it is invaded by the ventral plate, which is accompanied by the development of the intercostal vessels. In pigs' embryos this extensive membrane is also free from veins, with the exception of the zone encircling the cord, which again has a venous plexus more marked, however, than in the human embryo.

It appears, then, that during the third week of development, while the umbilical veins still empty into the sinus reuniens, an extensive plexus is formed throughout the greater extent of the membrana reuniens, which receives blood from the aorta on its dorsal side, and empties it into the umbilical vein on its ventral side. As the umbilical vein changes its position to enter the liver, this circulation through the membrana reuniens is broken up as the much earlier circulation through the umbilical vesicle was broken up.

The earliest collecting vein for the descending aorta is the omphalo-mesenteric vein ; next, it is the umbilical vein, and finally, when the abdominal walls are comjileted, it is the cardinal. This in turn is partly converted into the vena cava inferior.

The permanent arterial system is already well outlined in embryo II (Fig. 1). The aortic arches and segmental arteries are sufficiently well marked to permit one to number them. The vertebral artery is in process of development, it being formed by a union of a number of segmental arteries, as shown by His, by Froriep, and by Hochstetter. The seventh cervical segmental artery gives rise to the subclavian artery. The lower cervical, all the dorsal and lumbar segmental arteries, are concerned in the development of the thoracic and abdominal walls. Fig. 1 illustrates the extent of the arteries. It shows a simple arrangement from the vertebral to the hypogastric artery. The lower lumbar arteries are not shown. A section of this embryo is given in Fig. 2. It shows the relation of a segmental artery to the myotome. The segmental arteries supply primarily the spinal cord and ganglia by two groups of branches, one near the middle line and one more lateral. A more ventral group of segmental arteries supplies the Wolffian body. The blood from all these groups of arteries is collected by the cardinal veins.

The lateral group gives rise to the intercostal arteries by first supplying the myotome, and, as this grows into the membrana reuniens by a process of budding, the vascular loop follows it. In so doing the loop is first on the dorsal side of the sympathetic and finally on its lateral side, thus making the sympathetic cord cross the intercostal arteries and veins on their ventral side, as is the case in the adult.

No sooner has the vascular loop extended to the lateral side of the sympathetic cord than it begins to anastomose with neighboring segmental loops, as single vessels near the subclavian and hypogastric arteries, and as a plexus midway between these two. Tliis gives us at tliis early period a complete lateral anastomosis from the subclavian artery to the femoral, as Fig. 3 shows. It remains only for this system to shift around towards the median line with the muscle, nerves and ribs to form the condition of things as found in the adult.

Fig. 2. — Section through a human embryo lour weeks old (No. II). Enlarged 55 times. 4, aorta ; FW, foramen of Winslow ; MB, membrana reuniens; L, liver; R, heart.

Fig. 3 shows that the upper and lower segmental arteries of the series do not correspond at this early time with the same in the adult. Above, the superior intercostal is missing, while below, there is only a small fourth lumbar artery present, and it arises from the middle sacral. Iliolumbar and circumflexiliac arteries are altogether wanting, and I should judge from the relation of the arteries in this embryo, that the arch formed by the iliolumbar and circumflex-iliac is of secondary origin and has nothing to do with the segmental arteries. That they form anastomoses with the lower lumbar arteries in the adult can be explained in other ways.

The hypogastric artery is present long before the segmental arteries are formed near its junction with the aorta, and on this account we can no more call the trunk of the common iliac artery segmental than we can apply the same term to the descending aorta. We can only locate its origin in the neighborhood of the fourth lumbar artery.

Hochstetter has settled definitely that the subclavian is a branch from the seventh cervical segmental artery.* Between the seventh cervical and the third dorsal we have three segmental arteries. In Fig. 1 the segmental arteries in this region are all simple with the exception of the seventh, which sends a large branch into the arm. From this stage to the one pictured in Fig. 3 there is a jiimp, but in it we see the intermediate stage between Fig. 1 and the adult.

Fig. 3. — Arterial system of a human embryo six weeks old (No XLIII). Enlarged 5 times.

All of the arteries below the vertebral are destined to pass behind the sympathetic, and it is excluded only on account of its direction. In Fig. 3 the eighth cervical segmental passes on the ventral side of the nerve, which shows conclusively that it must either be a new artery or a secondary connection between the eighth segmental and the subclavian. Since the first and second intercostal arteries pass behind the sympathetic in this embryo and in front of it in the adult, we must accept Hochstetter's opinion that the superior intercostal is formed by secondary connections between the upper intercostals and the subclavian. If the old connection remains, it forms the arteria aberrans.

I stated above that the sympathetic lies in front of the subclavian, while in the adult it lies in a great part behind it. Hochstetter explains this change of position by a wandering of the trunk of the artery through the group of embryonic nerve cells. In earlyembryos the sympathetic system resembles a group of sprouts from the segmental nerves which cross the segmental arteries, and the sympathetic cord is of secondary formation. This cord grows very rapidly during the fifth and sixth weeks, to form a great mass of cells extending from the vagus ganglion to the adrenals, connecting all of the branches with the segmental nerves to make of them rami conmiunicantes. This all goes on hand in hand with the descent of the heart into the thorax. At the same time the arm is rotating towards the ventral median line, and drags with it the subclavian artery. In so doing the subclavian is dragged into the sympathetic cord in its earliest stage, thus allowing the greater portion of the cord to be developed on its dorsal side. The portion of the sympathetic which from the first lies on the ventral side of the subclavian becomes the ansa subclavia.

  • Hochstetter numbers the segmental arteries to correspond with the vertebrK above them. Throughout I number the arteries with their accompanying nerves. He states that the subclavian arises from the sixth segmental, this being the same artery that I call the seventh cervical segmental.

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 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.

The simple diagram, Fig. 4, shows the origin of the main ai'teries of the trunk from the aortic arches and segmental arteries. This compared with Figs. 1 and 3 will explain itself. In the diagram the vessels which remain are black ; those which disappear, outlined; and those new formed, striated.

Resume : — While the aortic arches are forming, the arteries arising from the descending aorta pass on the mesial side of the coelom to the umbilical vesicle, and the blood passing through them is collected by the omphalo-mesenteric veins. Soon the segmental arteries arise, unite and shift backwards in the head region to form the vertebral artery. In the trunk they also unite within the lateral body-wall to form the internal mammary and deep epigastric arteries. Thisanastomosing arch, lying immediately below the tips of the ribs and the rectus abdominis muscle, wanders with them to the ventral middle line, the commrinicating branches forming the intercostal arteries. The whole course of the anastomoses between the tips of the segmental arteries takes on in its wandering the shape of the letter

Z (Fig. 4), the upper angle marking the origin of the subclavian. With the rotation and descent of the arm the subclavian is dragged partly through the sympathetic cord ; the origin of the superior intercostal is shifted, by the formation of a new anastomosis, from the dorsal to the ventral side of the sympathetic cord.

Fig. 4. — Diagram to show the development of the arteries of the trunk from the aortic arches and segmental arteries. The arteries which remain are black; those which degenerate are outlined; those newly formed are striated. /. C, internal carotid; E. C, external carotid; J?. A., bulbus aortae ; P., pulmonary artery; A. D., descending aorta; v., vertebral; S., subclavian; F., femoral; C, umbilical; 7, seventh cervical; 3 and 12, third and twelfth dorsal.

The first vein collecting the blood from the abdominal aorta is the omphalo-mesenteric ; next the umbilical, and finally, the cardinal assumes this function.

Cite this page: Hill, M.A. (2020, July 2) Embryology Paper - Development of the internal mammary and deep epigastric arteries in man (1898). Retrieved from

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