Paper - On the development of the superficial lymphatics in the skin of the pig

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Sabin FR. On the development of the superficial lymphatics in the skin of the pig. (1904) Amer. J Anat. 3:183-196.

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This historic 1904 paper by Sabin described pig lymphatic system development.


American .Journal of Anatomy. Vol. III.

Sabin FR. The lymphatic system in human embryos, with a consideration of the morphology of the system as a whole. (1909) Amer. J Anat. 9(1): 43–91.

Sabin FR. Description of a model showing the tracts of fibres medullated in a new-born baby’s brain. (1911) Amer. J Anat. 11(2): 114- .

Modern Notes pig | integumentary | immune

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On the Development of the Superficial Lymphatics in the Kkin of the Pig

Florence Rena Sabin (1871 - 1953)
Florence Rena Sabin (1871-1953)


Florence R. Sabin

Associate in Anatomy, Johns Hopkins University.

With 7 Text Figures. (1904)

  • This paper together with one on the Development of the Lymphatic System and a part of a paper on the Development of Lymph Glands, soon to appear in this Journal, was accepted by The Association for Maintaining the American Woman's Table in the Zoological Station at Naples and for Promoting Scientific Research by Women.

In a previous paper^ has been given an aecoimt of the origin of the lymphatic ducts from the veins by the budding off of blind sacs from their endothelial lining. The growth of these blind ducts toward the skin and their gradual spreading over the surface of the body was described briefly and illustrated by a composite picture. In the present communication the spreading of the superficial lymphatics will be described more in detail as well as the growth of these ducts in the different layers of the skin.

  • On the Origin of the Lymphatic System from the Veins and the Development of the Lymph Hearts and Thoracic Duct in the Pig. The American

The lymph ducts bud off from the veins in four places; two in the neck, at the junction of the jugular and the subclavian veins; and two in the posterior part of the body, from the vein Avhich enters the Wolffian body and which is formed by the union of the femoral and sciatic veins. As the Wolffian body dissappears, and its venous system is supplanted by the vena cava, this lower connection of the lymphatics with the veins is given up. From these four points of origin the lymphatics grow first along the veins toward the skin, and secondly along the aorta and its branches to the various organs. The superficial lymphatics to the skin follow the veins, the jugular in the neck and the femoral and its branches in the lower part of the body. The deep lymphatics follow the arteries ; primarily the aorta making the thoracic duct, and secondarily the branches of the aorta.

In embryo pigs below 18 mm. in length there are no lymphatics in the skin, as has been proved both by numerous negative injection experiments and by their absence in serial sections. The first sign of the lymphatic system was found in a pig 11.5 mm. long. It consisted of two small blind ducts which had budded off from the vascular endothelium at the junction of the cardinal and subclavian veins on either side of the neck. These ducts were found to grow into the neck along the anterior cardinal or jugular veins to a point midway between the ear and the scapula, and here widened into a sac. This sac, though possessing a lining of a single layer of endothelial cells without a muscle coat, I have considered to be analogous with the lymph hearts of the amjDhibia. From the sac the ducts grow directly outward to the skin, which they reach when the pig is 18 mm. long.

In Figs. 1 to 5 is given a series of actual injections of the lymphatic ducts in the skin of pigs of increasing sizes. Each picture is a drawing from one actual injection, and all of the injections are practically complete except Fig. 3. That is to say, there are no lymphatics in the skin at these various stages excepting those which are shown injected. The methods of these injections are given in the paper cited above.

Fig. 1 represents the lymphatic ducts in the side of the neck of a pig 2.5 cm. long, and shows that the ducts are growing in two directions, first over the back of the head behind the ear, and secondly over the scapular region. In Fig. 2, from a pig 3 cm. long, these two tufts of lymphatics, one behind the ear and the other over the scapula, are more distinct and have increased in complexity. A new set of ducts has reached the surface at the angle of the jaw and has begun to grow out in two directions, first between the eye and the ear, and secondly in front of the eye.

Fig. 3, from a pig 3 cm. long, does not show the entire lymphatic systern of the skin of a pig of that stage, for the ducts at the angle of the jaw are not injected, nor a set of ducts which has just reached the skin over the crest of the ileum. This group of lymphatics is shown farther developed in the next figure. Fig. 3, however, does show the primary set of ducts, that is, those that grow over the back of the head and slioulder completely injected. It brings out clearly the character of the plexus, the irregularity of the ducts and the fine channels that connect neighboring wide ducts. It shows also the growing sprouts that run out in advance of the plexus to invade new areas of the skin, areas which up to this time have had no lymphatics.

Fig. 1. The lymphatic system in the skin of a pig 2.5 cm. long, x 3.

Fig. 2. The lymphatic system in the skin of a pig 3 cm. long. x3.

In Fig. 4, from a pig -i.3 cm. long, the ducts of the primary plexus have grown to the median line in the back and, anastomosed with those of the other side. The ducts over the face are well injected. The figure shows also that the lymphatics for the lower part of the body have reached the skin at a point over the crest of the ilinni. From this point the ducts radiate to the skin over the side, back and liip. From no other center of radiation for the primary lymphatics do the ducts spread out so symmetrically, so like the spokes of a wheel, as in this case. In the neck there are several centers of radiation, so that no one center sends out ducts in every direction.

Fig. 3. A partial injection of the Ij^mphatic system in the skin of a pig long. The primary group of ducts is completely injected. X 3.

Fig. 5, from a pig 5.5 cm. long, is the last of the series. The injection was made by two insertions of the hypodermic needle, one over the scapula with the needle opening toward the neck, and the other just below the point of radiation over the crest of the ilium. In this way one takes advantage both of the radiating direction of the ducts and of the larger

size of the primary ducts. The ease of injection in any direction shows that there are no valves at this stage, though the flow of any injection

Fig. 4. The lymphatic system in the skin of a pis -l-S em. lonj;. x 3.

mass is irregular on account of tlie great variation in the size of the channels. In making these injections it is essential to enter the needle into the level wliich contains the lymphatics. As will be shown later.

Fig. 5. The lymphatic system in the skiu of a pig 5.5 cm. long. X 3.

this level is the line between the subcntaneous tissue and the chorium. When the needle enters the subcutaneous tissue in pigs from 3 to 8 cm. long the injection mass spreads out in straight lines and forces a path for itself in the tissue spaces. When the needle enters the chorium the injection mass raises a bleb on the surface. In neither of these cases, that is, when the injection mass has entered the tissue spaces of the subcutaneous tissue or of the chorium in small embryos, have I ever succeeded in getting a lymphatic injection. To obtain a perfect injection without any extravasation at the point of puncture one must enter the needle at exactly the right level, that is, between the subcutaneous tissue and chorium and then inject slowly. One then sees the ducts starting out from the open slit in the injection needle. By giving a scarcely perceptible pressure on the piston of the hypodermic syringe it is possible to inject the entire side of the embryo and have the individual ducts leading from the needle stand out clearly at the end, that is, to have no extravasation. Thus it will be noted that it is necessary to puncture the ducts in order to get a lymphatic injection.

In Fig. 5 the ducts have covered the body and only the feet, a part of the head and the tail remain unsupplied. It will be noted that the' ducts from the different centers in the neck have anastomosed so freely in the skin that it is not easy to see just where the primary points of radiation lie. Moreover, the ducts for the anterior part of the body have anastomosed so freely over the surface of the body with those for the posterior part that it is possible to inject into the ducts over the ilium and have the injection mass pass toward the veins in two ways; first through the ducts that come to the surface over the crest of the ilium, and secondly by an indirect course through the channels over the side of the body to the ducts in the neck.

In a pig 6.5 cm. long the spreading of the superficial lymphatics in the skin is practically completed. That is to say, ducts have been injected to the top of the head, the snout, the ears, eyelids and toes. In these areas, far from the centers of growth, the plexus of ducts is not abundant at this stage, indeed, to use one area as an example, only a few of the advance sprouts over the top of the head have actually anastomosed with the ducts of the other side. However, no area of the skin is wholly without lymphatics. In other words, the invasion of the skin by lymphatics is complete though the plexus of lymphatics in the skin is very incomplete.

To sum up : In the anterior part of the body there are three main centers from which the superficial ducts spread out; first, in the posterior part of the neck, for the ducts over tlie back of the head and over the scapula; second, at the angle of the Jaw, for the ducts of the face; third, in the front of the neck, for the ducts of the lower jaw, chest and fore legs. Tlie ducts of all these systems anastomose freely in the skin. In the' posterior part of the hody there are two centers for the radiation of the ducts, first over the crest of the ilium for the ducts of the posterior part of the back and of the hip, and secondly in the inguinal region for the ducts that grow into the abdominal wall and down the leg. The ducts of the anterior and posterior systems anastomose freely over the body.

Having traced the spreading of the superficial lymphatics in the skin from the time the ducts first come to the surface in the neck and over the crest of the ilium to the time when they have reached the remotest parts of the body, namely, the top of the head and the tips of the toes, it remains to trace the development of these ducts in the different layers of the skin.

In pig embryos 13 mm. in length the epidermis is from two to four cells deep and is separated from the connective tissue beneath by a distinct basement membrane. The connective tissue beneath is loose or compact in different parts of the body, and is not divided into layers, so that there is no differentiation between the chorium and the underlying subcutaneous tissue. The blood capillaries in this connective tissue are large, having a width of from two to four or five times the diameter of the red blood corpuscles, which at this stage are large nucleated cells.

By the time the embryo is 15 mm. long, a stage just about the time that the lymphatics are budding oft" from the veins but before they have reached the skin, there are certain areas of the body, for example, over the arm bud, where the connective tissue beneath the epidermis is divided into two distinct layers, a denser layer next the epidermis and a looser meshed layer just within. The outer, denser layer is to become the chorium, and the inner, looser layer the subcutaneous tissue. The blood capillaries lie at this stage on tlie inner border of the chorium between it and the subcutaneous tissue. There are numerous vessels in the subcutaneous tissue but none in the true skin.

Soon the blood capillaries begin to grow outward into the chorium and give up their position along its inner border. The vessels in the subcutaneous tissue remain and become larger, iis the blood capillaries advance into the true skin the lymphatic capillaries grow in just behind them, taking the position along the inner border of the chorium. In an embryo 3 cm. long the lymphatic capillaries lie in this border just internal to the blood capillaries. Fig. 6 shows the lymphatics in the skin over the shoulder of a pig 5 cm. long. It will be noted that there is a clear differentiation between the choriiim and the subcutaneous tissue. In the chorium the protoplasmic network is fine and closely meshed, while the subcutaneous tissue is more fibrillar, the tissue is more open or the spaces are larger. The lymphatics are large and lie in the border between the chorium and subcutaneous tissue. The blood capillaries are small

Fig. 6. Transverse section of the skin of the shoulder of a pig 5 cm. long showing the primary lymphatics. About X 110. he; blood capillaries; c, chorium; I, lymphatics ; st, subcutaneous tissue.

and lie both in the subcutaneous tissue and in the chorium. All of the vessels within the chorium are confined to its inner half.

From this time on. until the embryo is 6.5 cm. long, the lymphatics gradually spread over the entire body in a single layer of ducts. These ducts make a characteristic plexus, as shown in Fig. 5. The plexus has been described and illustrated in the paper cited above. The growth of the ducts within the plexiis has been described by Eanvier " and by MacCallum/ The original discovery of this method of growth was made, not by Eauvier, as I stated in a previous paper, but by Langer* in 1868. At the time of my first publication I had not seen Langer's paper. He published a series of papers on the lymphatic system of the frog, and in one of them on the lymph vessels in the tadpole's tail, he gives beautiful pictures of the lymphatics, with their complete lining of endothelium and with the long sprouts of endothelial cells from their walls. Some of the sprouts he shows as still solid, others partly injected. He recognized that this represents the method of growth; moreover, he states that without doubt the lymph capillaries and the blood capillaries develop in the same way — their elements being the same.

^Ranvier: Comptes Rendus, 1895 and 1896. Archiv d'Anatomie, 1897. 'MacCallum: Arch. f. Anat. u. Phys., Anat. Abth., 1902.

The plexus of growing lymphatics is well seen when the freshly injected skin of the embryo pig is stripped off and examined under a binocular microscope. It can thus be made out that the ducts spread out practically in one plane.

By the time the pig is 8 cm. long an injection of the lymphatics shows the primary plexus well developed. Many of the vessels are large and the plexus is wide meshed. At the same time the skin viewed under the binocular shows that there are numerous sprbuts from the primary plexus which are growing outward into the chorium. These small, new sprouts do not as yet make a perfect plexus within the chorium. Sections of the skin at this stage bring out three points: First, that the ducts of the primary plexus now lie deeper in the subcutaneous tissue rather than just in the border between the subcutaneous tissue and the chorium. Secondly, that there are a few lymphatic vessels within the chorium; and, thirdly, that the blood capillaries are nearer the surface of the skin than the lymphatics.

By the time the pig is 10 or 11 cm. long the lymphatic capillaries within the chorium have become a complete plexus. Viewed under the binocular microscope, there are now two distinct layers of lymphatics, a deeper plexus with wide spaces between the ducts and a more superficial plexus of finer ducts more closely crowded together. In sections the deeper plexus is subcutaneous, while the superficial lies about the middle of the chorium. The complexity of the plexus varies greatly in different parts of the body, for example, there are many more lymphatics in the ear than in an area of skin of equal size over the back. The stages of development are given for the skin over the shoulder, the development in the remoter parts, for example, in the feet, is always somewhat retarded.

â– â– Langer: Die Lymphgefasse im Schwanze der Batrachier-Larven. Sitzb. d. k. Akad. d. Wissensch., I. Abth., Juli Heft, Jahrg. 1868.

While the pig is increasing from 10 to "35 em. in length the two lymphatic plexuses, the deep or primary and the superficial or secondary, become more complicated. Valves begin to develop in the lymphatics and increase the difficulty of obtaining lymphatic injections. By the time the embryo is 16 or 18 cm. long the valves are present and prevent much backward injection. At this stage, and still more clearly in pigs between 20 and 25 cm. long, a subcutaneous injection of considerable pressure will usually enter the deep plexus of lymphatics and run centralward in the ducts of the subcutaneous tissue, but not outward into the plexus of the chorium. This is readily demonstrated by injecting into the foot' pads. If the injection is in the hind feet the fluid enters the ducts of the subcutaneous tissue and is carried to the inguinal glands; if in the fore feet, the ducts lead to the glands in the front of the neck. A subcutaneous injection then in a pig about 20 cm. long enters the deep lymphatics. The injection mass, however, often enters the chorium, not in the superficial lymphatic plexus, but rather through certain veins that run directly to the surface and spread out in a fine plexus just beneath the epidermis. These vessels are blood capillaries, as can be proved by making a venous injection. Prussian-blue was injected into the umbilical vein of a pig 22 cm. long, under a pressure of 100 mm. of mercury. The skin soon showed fine points of blue, and each point was seen to be a fine plexus of ducts just beneath the skin, the plexus spreading out from a small vein which ran to the surface. Thus, since by subcutaneous injections in these stages one usually gets a mixed injection of deep lymphatics and superficial veins, the lymphatics are best studied by complete venous injections.

Fig. 7 is a section of the skin of the ear of a pig 22 cm. long in which Prussian-blue was injected into the umbilical vein under a pressure of about 100 mm. of mercury. The veins are filled with blue granules, the capillaries with blood corpuscles, while the lymphatics are empty. The epidermis is now several layers deep, the hairs are partly developed, but there are no papillae. There is still some differentiation between the subcutaneous tissue and the chorium, the former being more fibrillar and having wider spaces, the latter being denser and more cellular. The lympliatics are not as large as in earlier stages and they lie in two planes, a primary plexus of ducts in the subcutaneous tissue and a secondary plexus in the chorium.

To complete the study of the development of the ducts in the skin it was necessary to find out wliether the lymphatic capillaries enter the papillae or not. The papilla are present in the skin of the new-born pig, but the hairs make the skin so diflficnlt to study that the papillae are best seen in the tongue. By making a complete arterial injection and forcing the injection mass over into the veins of a pig a week old, it was easy to demonstrate the lymphatics in the subpapillary layer and

Fig. 7. Skin of the ear of a pig 22 cm. long. Tlie veins are injected with Prussian blue represented as black. About x 05. a, arteries ; be, blood capillaries ; c, chorium ; Vl, primary lymphatics ; si, secondary lymphatics ; si, subcutaneous tissue, v, veins.

in the center of the larger papilla. The smallest papillae contain just a tuft of blood capillaries in the center, while the larger ones at the side of the tongue have a central artery which is bordered by a central lymphatic duct lined with epithelium. This makes the papillse in the tongue analogous with the villi of the intestine as far as the central lymphatic duct is concerned.

Thus the course of the development of the lymphatics has been followed in the skin. The ducts are defined as channels with an endothelial lining which bud off from previous lymphatic ducts, the original ones coming from the endothelium of the veins. The development has been traced by making injections along the lines in which the lymphatics grow to the skin. In the neck the ducts grow toward the skin along the jugular vein and come to the surface at three points; in the posterior part of the neck, at the angle of the jaw and in the front of the neck. In the posterior part of the body the ducts follow the femoral and its branches and come to the surface first over the crest of the ilium, and secondly in the inguinal region. From these points the ducts invade the skin and form a primary plexus in the subcutaneous tissue and a secondary one in the chorium. From the plexus in the chorium sprouts grow outward into the center of the papillae. In their entire growth the lymphatics follow the blood vessels.

The lines of growth of the lymphatics to the various organs are along the course of the aorta and its branches. For example, by injecting into the edge of the wall of the aorta it is possible to inject the ducts as they are entering the heart and the lungs. The early ducts to the kidney are large and easy to olitain. By the time the pig is 4 cm. long the ducts can be injected to the stomach wall and have grown between the folds of the mesentery to the intestinal wall. Repeated injections would probably show tlie growth of the ducts into the different layers of the intestinal wall to their end in the central chyle vessel of the villi.

Cite this page: Hill, M.A. (2020, June 5) Embryology Paper - On the development of the superficial lymphatics in the skin of the pig. Retrieved from

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