Paper - On the origin of the abdominal lymphatics in mammals from the vena cava and the renal veins (1912)

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Sabin FR. On the origin of the abdominal lymphatics in mammals from the vena cava and the renal veins. (1912) Anat. Rec. 6(8): 335-343.

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This historic 1912 paper by Sabin describes the origin of the abdominal lymphatics in mammals.

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On the Origin of the Abdominal Lymphatics in Mammals from the Vena Cava and the Renal Veins

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

Florence R. Sabin

From The Anatomical Laboratory, The Johns Hopkins University


It is a pleasure to have for study Mr. Kampmeier's able and valuable paper on the thoracic duct, as seen in one of my specimens, in the June number of The Anatomical Record. His direct dorsal view of a wax reconstruction of the jugular lymphatics brings out one point better than my profile reconstruction sho^vn to the American Association of Anatomists in 1910. This point is the crossing of the thoracic duct to the right side which I have often, though not always noted, in injections of later stages. Moreover, his paper is a clear and excellent presentation of the theory of the growth of lymphatics by the addition of tissue spaces.

My own work on the thoracic duct is to appear in a forthcoming number of the Ergebnisse ftir Anatomic unci Entwicklungsgeschichte, but I should like to present this preliminary note.

Lymphatics in mammals arise in two places, (1) from the anterior cardinal veins in the neck, (2) from the inferior vena cava and the adjacent veins of the Wolffian bodj' or kidney. The budding of the jugular lymphatics is from the anterior cardinal veins near the duct of Cu\^er but is not strictly limited to the anterior cardinal veins. In different forms the budding may extend along some of the adjacent veins, nameh' the posterior cardinal, the primitive ulnar and the capillaries that eventually make the root of the external jugular vein. The lymphatics which bud off from the inferior vena cava, which is a part of the large vein which connects the two Wolffian bodies, and from some of the veins in the edge of the Wolffian body grow in three directions. Those that grow ventral to the aorta make the retroperitoneal sac ; those that grow caudalward, lateral to the aorta, make the iliac sacs; and those that grow dorsal to the aorta make the cisterna chyli and the lower part of the thoracic duct. There are therefore two pairs of symmetrical primary sacs in mammals, the jugular and the iliac, and two median sacs, the retroperitoneal and the cisterna chyh. It might be said that there are three dijfferent sacs in mammals, the jugular (paired), the iliac (paired) and the retroperitoneal (unpaired) and these three sacs are comiected A^th each other by the cisterna chyli and the thoracic duct. However as I shall define primary lymph sacs as those which bud directly off from the veins, it is necessary to include the cisterna chyli with the primary lymph sacs. The primary lymphatic sacs and the thoracic duct make the primary lymphatic system.

The thoracic duct arises in part as a cIoaati growth from the left jugular lymph sac and in part from a plexus of h'mphatics which buds off from the veins of the Wolffian bod}'. While the thoracic duct is incomplete, it is excessively hard to inject. The specimen which I loaned to Mr. Kampmeier is not a perfect injection since it has extravasations; it is, however, the first and until the past month the only injection ever made of a mammalian thoracic duct before it is complete. It was made indirectly through the jugular sac. I filled the sac with ink and then bent the head forward and to my surprise the ink shot into the thoracic duct. As will be readily seen an injection into the jugular sac almost invariably runs by the path of least resistance or the physiological path into the veins and does not back into the thoracic duct. Perfect injections of lymphatic capillaries wthout and extravasations can be made, as for example Mrs. Clark's injection of the jugular lymphatic plexus in the chick shown on page 263 of the June number of The Anatomical Record for this year, 1912, but to obtain perfection it is necessary to watch the entire field of injection under the microscope in order to regulate the pressure.

Mr. Kampmeier's figure 1 shows the jugular portion of the thoracic duct which arises as sprouts from the jugular sac. These sprouts form a plexus dorsal to the esophagus from which ducts grow downward. The shorter left duct follows the vein to the root of the heart and I think subsequently grows to the left side of the heart and the left lung. A longer duct crosses to the right side and is the upper thoracic part of the thoracic duct.

The abdominal portion of the thoracic duct in the pig buds off from the two sides of the large vein which connects the Wolffian bodies and forms part of the vena cava and from the large veins in the capsule of the Wolffian body itself. Dr. and Mrs. E. R, Clark have shown in the June number of The Anatomical Record for 1912 that the lymphatics for the posterior lymph hearts of the chick bud off from the coccygeal vein and its branches, and these lymphatic buds are filled with stagnant l)l(t()(l by a Wick How from the parent vein. These lymphatic buds first make a plexus out of which the lymph heart is formed. In the chick the lymphatics while they are still iu the blood filled staf;-ef:;rowout toform the peripheral capillaries in the skin. Moreover they are closed vessels, first because the blooil in them is hekl within the contour of the vessel, and secondly because a little ink injected into one vessel will fill the entire lymphatic system aiul empty into the veins without any extravasation.

In reworking all of the sacs in the pig, I have found that the primary buds are packed with blood (fig. 7 in 14) and that the l)lood empties gradually so that the sacs are subsequently partially filled and finally empty. The jugular lymphatics bud off from the jugular veins making the well known jugular sacs. All the rest of the tymphatics in the pig bud off from the mesonephritic veins. The retroperitoneal sac comes oft" from the ventral surface of the mesonephritic vein in the midline of the embryo. I found out the fact that the abdominal part of the thoracic duct comes from the same vein by direct puncture of the cisterna chyli in the blood filled stage. I saw the ink enter the mesonephritic vein. I have three injections of the abdominal sacs or rather plexuses made in embryos 23 mm. long. No one of them is perfect and none shows the cisterna chjdi since the ink around the point of injection obscures it. They all show that the beginning thoracic duct, two symmetrical plexuses along the edge of the Wolffian body and the retroperitoneal sac comiect. I shall subsequently describe these injections more in detail when I can also present views of the veins of the region as well. For the present I want to describe the blood filled hnnphatic buds as they appear in 23a which Kampmeier studied, as well as in another specimen from the same litter and in a human embryo of about the same stage.

In the series 23a, which measured 23 mm. in its greatest length in the fresh specimen the blood packed lymphatic buds are to be seen in sections at the level of the median mesonephritic vein. They are in the angle between the vein and the mecUo-dorsal edge of the Wolffian body. These buds while still packed wdth blood form (1) the iliac lymphatics and (2) the cisterna chyli. In a series measuring 22 mm., I have found the -earliest blood filled iliac buds arising from the large veins in the capsule of the Wolffian body, as well as the dorso-lateral surface of the mesonephritic vein near the Wolffian body. In 23a the iliac plexus of blood packed lymphatics has grown caudalward along the dorso-medial border of the Wolffian body as far as the hilum of the permanent kidney. This plexus of blood filled lymphatic capillaries is spreading out in the capsule of the kidney and in later stages I have injected a plexus of lymphatic vessels from the iliac sac into the hilum of the permanent kidney around its pelvis. This explains why the permanent kidney is supplied by iliac lymphatics, while on the other hand the retroperitoneal sac spreads into the ventral capsule of the Wolffian bodies as far as the edge of the reproductive glands. Their lymphatics therefore grow from the retroperitoneal or prae-aortic sac.

The iliac sac is not complete in 23a; the iliac plexus grows down to a point exactly opposite the bifurcation of the aorta where it swells into a sac which I first identified as the posterior sac in 1901 in an embryo pig 25 mm. long. From this enlarged end grow three main groups of lymphatics, (1) an abundant plexus of vessels surrounding and following the umbilical arteries, (2) the femoral and (3) the ilio-lumbar vessels which together drain the leg and abdominal wall.

The cisterna chyli is not present in 23a, but in an embryo 23b from the same litter as 23a, the blood filled plexus which arises on either side in common with the iliac plexus has arched across the midline, dorsal to the sympathetic ganglia and the aorta. Immediately dorsal to the aorta at the level of the anlage of the adrenal bodies the blood filled lymphatics have enlarged into a cisterna chyli. In my article in the Ergebnisse I have shown this important point, that all of the primary lymphatics bud into non-vascular zones; if the non-vascular areas are large, the sacs are large, as for example the jugular and the retroperitoneal sacs in the pig; if the non-vascular areas are small, the sacs are small, as for example the iliac sac and the cisterna chjdi in the pig. The cisterna chyli develops opposite the adrenal anlage just at the tip of the developing azygos veins. Caudal to this point the segmental venous plexus drains through the Wolffian body and the transition zone is a small non-vascular area. Tracing the thoracic duct by the presence of the blood, the vessels have not yet grown beyond the region of the adrenal bodies, the blood filled plexus has, however, grow caudalward dorsal to the aorta to a point opposite the hilum of the permanent kidney.

The rest of the thoracic duct forms rapidly, and is probably complete at the stage measuring 25 mm. I have completely reconstructed it at 27 mm. The lower segment is always characterized by being an exceedingly abundant pk^xus which surrounds the aorta as is shown in Pensa's figures (11), while the portion from the heart to the neck is often a single trunk or at least a few vessels. In a third s]:)e('imen measuriu^ 2;^ mm. in w liicli I washed out the Mood vessels with J.oeke's sohitioii, tlie aluloiuinal lymphatics are partially filled with blood and the veins are empty. This shows that the ])lood packed stage is a short one. In this specimen lymphatics from the retroperitoneal sac are growing; around the aorta to connect with the cistema chyli. Subsequently the main connection is around the cerebral surface of the adrenal. All of the abdominal sacs l^ecome connected with each other.

A new embryo in the Mall collection, No. 460, measuring 21 mm. is of great interest in connection with the abdominal lymphatics. A careful reconstruction of this specimen with abundant illustrations will be of value, but for the present I can only give a brief description. I injected the embryo with India ink through the umbilical artery while the heart was still beating. The vascular injection is almost perfect. The embryo was then put directly into bichloride-acetic and the fixation is excellent.

In marked contrast to the embryo pig of about the same length the Wolffian ])odies are disappearing, being pushed caudahvard by the growing permanent kidneys. The cerebral pole of the Wolffian bodies, now far to the side, lies opposite the large median vein which still drains the Wolffian bodies. This vein is now markedly assymmetrical, owing to the enlargement of the right side of it, due to the vena cava. From the sides of the median vein extends a plexus of veins to the permanent kidneys.

From the ventral surface of this vein in the midline is a group of blood filled lymphatic buds, lying in the root of the mesentery This area is very small in the human embryo, in marked contrast with the large area of the pig, and the human retroperitoneal or pre-aortic sac is consequently of small size. It is of considerable interest to note that the connective tissue near these hTiiphatic buds has wider spaces than along the rest of the border of the vein. They can, however, be distinguished from the lymphatics. Some lymphatics are growing from the dorsal surface of the median vein, and, pushing between the masses of cells of the sj-mpathetic ganglia, have reached the ventral surface of the aorta.

The iliac lymphatic sacs are of great interest. They are farther advanced than the retroperitoneal sac, because (1) they are larger and (2) they are only partly filled with blood. They arise not from the veins of the Wolffian body but from the veins of the permanent kidney. Along the dorso-medial l)order of the kidneys between the kidney and the segmental veins are two long sacs, the one on the left being about 1.8 mm. long. The left sac reached the bifurcation of the aorta; the caudal part of the right sac is less developed, and the place for it is small, on account of the size of the vena cava. Instead of a sac there are some blood packed buds along the vena cava itself.

The cerebral ends of the iliac sacs meet in a small plexus of blood filled vessels dorsal to the aorta opposite the adrenal bodies. This marks the position of the future cisterna chyli. The abdominal part of the' thoracic duct can be traced for some distance in the sections. The trmik for the jugular sac is present but I do not think that the two parts have met. Another point of great interest in the specimen is that it shows many areas of widened tissue spaces along the aorta. They can, however, be distinguished from the lymphatics.

The question at issue between Mr. Kampmeier and myself is the method of gro'W'th of the thoracic duct between the two anlagen, the jugular and the renal segments. I admit at once that I have not seen the duct grow in the living form, nor have I mastered the difficulties of injecting it so as to demonstrate its gradual growth from two venous anlagen. The isolated spaces shown in INIr. Kampmeier's figure 1 , I submitted to most careful study before the meeting in 1910 and discussed them there; they are endothelial lined and I believe them to be lymphatics. I believe that adequate injections would show that they connect with the rest of the system. It was these vessels which made me consider whether the origin of the thoracic duct was not from a series of vessels from the azygos veins, but this point has now l^een cleared up by finding that the cisterna chyli arises as blood filled buds from the mesonephritic or renal veins. The fact that the injection mass extravasatedjustaljove the long apparently isolated lymphatic on the right side is not an unsurmountable difficulty, for it has l)een noted by a long list of observers among whom are Sigmund Mayer (9), Ranvier (12), MacCallum (8), Bartels (1) and myself (13) that it is an especial characteristic of lymphatic capillaries that tiny sprouts in which extravasations may readily occur often lead to wide sacs or vessels. In fact both Strieker (16) and Sigmund Mayer have seen blood capillaries contract down to a thread in a living tadpole's tail, so it is known that endotlu^lium is contractile.

In regard to the method of growth of the intermediate division of the thoracic duct, I know that the peripheral lymphatic capillaries grow by budding of their endothelial wall, having seen them in the Hving tadpole, I know that the lymphatics in the chick bud off from the veins and grow to the peripheral capillaries in skin as closed eudolhelial vessels li;niiifi st'cu lliciu in the Clark's specimens. I know as nearly as ])()ssihlo withoul actually seeing hee process in the living form, that the thoracic duct l)ogins in mammals as a clown growth from the jugular sac and as an up growth from the cisterna chyli which comes from the megonephritic or renal veins, I therefore do not believe that its further growth is by a process different from the rest of the lymphatic and blood vascular systems.

The discovery that all the al)dominal lymphatics in mammals come from the veins of the AVolffian body or kidney brings out the significance and the importance of Silvester's (15) beautiful injections in South American monkeys. He showed that in this one form the renal connections are permanent. It also allows us to consider the question of the relation of the mammalian lymph sacs to the lymph hearts and sacs of the amphil)ia. The anterior lymph hearts of the amphibia bud ofi from the vertebral veins (Knowcr (7) and Hoyer (5)) and as Knower has shown gets its muscle from the myotomes ; the posterior lymph hearts of amphibia and birds arise from the coccygeal veins, they lie against the myotomes and have muscle in their walls. The anterior lymphatics of birds and mammals arise from the anterior cardinal vein and do not develop muscle. The abdominal lymphatics of mammals bud off from the renal veins and form three sacs, the retroperitoneal, the iliac and the cisterna chyli. These sacs are like the amphibian lymph hearts in their most fundamental point, namely that they bud directly- from the veins, the}^ differ from them in position not lying against the myotomes and in not developing muscle. They are not analogous to the amphibian lymph sacs which are secondary structures, transformed from lymph ducts. The mammalian sacs therefore might be called primary Ijnmphatic sacs. As a matter of fact the following is the embryological classification. Primary lymph sacs: (a) those which develop muscle in their wall, forming true lymph hearts, for example the anterior and posterior lymph hearts of amphibia and the posterior lymph hearts of birds; (b) those which do not develop muscle, but become partially transformed into lymph glands, for example the jugular lymph sacs of birds and mammals and the mesonephritic (renal) lymph sacs of mam.mals. In a word, primary lymph sacs may become lymph hearts or h'lnph glands.

Literature Cited

(1) Bartels, p. 1909 Das Lymphgefasssystem. Bardeleben's Handbuch der Anatomic des Menschen. Fig. 9.

(2) Baetjer, W. 1908 Amer. Jour. Anat. vol. 8.

(3) Clark. E. L. 1912 Anat. Rec. vol 6, p. 247 and p. 261.

(4) Clark, E. R. and E. L. 1912 Anat. Rec, vol. 6, p. 253.

(5) HoYER, H. 1908 Bull, de L'Acad. des Sciences de Cracone.

(6) Kampmeier, O. 1912 Anat. Rec, vol. 6.

(7) Knower, H. McE. 1908 Anat. Rec, vol. 2.

(8) MacCallum, W. G. 1902-03 Arch. f. Anat. und Phys., Anat. Abth., and Bulletin of the Johns Hopkins Hospital, vol. 14.

(9) Mayer, Sigmund 1885 Sitzungsber. der k. Akad. der Wissenshaften Wien, Abth, 3, Bd. 91 and 92.'

(10) McClure, C. F. W. 1912 Anat. Rec, vol. 6.

(11) Pensa 1908-1909 Lab. di Anat. norm, della Univ. di Roma, T. 14.

(12) Ranvier 1897 Arch. d'Anat. microscopique, T. 1.

(13) Sarin, F. R. 1901 Amer. Jour. Anat., vol. 1.

(14) 1909 Amer. Jour. Anat., vol. 9.

(15) Silvester, C. F. 1912 Amer. Jour. Anat., vol. 12.

(16) Stricker 1865 Sitzungsbr. der Math.-Naturwissen. Classe d. k. Akad., Wien.

Cite this page: Hill, M.A. (2021, May 11) Embryology Paper - On the origin of the abdominal lymphatics in mammals from the vena cava and the renal veins (1912). Retrieved from

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