Paper - An anomaly of the thoracic duct with a bearing on the embryology of the lymphatic system (1915)

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Clark ER. An anomaly of the thoracic duct with a bearing on the embryology of the lymphatic system. (1915) Contrib. Embryol., Carnegie Inst. Wash. 2: 45-54.

Online Editor Note 
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This historic 1915 paper by Clark is an early description of the early development of the thoracic duct abnormality.

Modern Notes:

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An Anomaly of the Thoracic Duct with a bearing on the Embryology of the Lymphatic System

Contributions to Embryology, No. 3.

By Eliot R. Clark,

Professor of Anatomy, University of Missouri.

The case which is to be described has an exceptional interest, both because of its rarity and because of the bearing which it has on the still unsettled problem of the mode of develop- ment of the thoracic duct. It occurred in a dissecting-room subject, in a negro female (No. 3408 in the dissecting-room series of the Johns Hopkins Medical School), aged 39 years, of slight build, distinctly below the average in height, weighing only 102 pounds, whose death was due to "tuberculosis" (a diagnosis borne out by the condition of the lungs noted in the course of dissection). Thanks are due to Miss Goldman, Mr. Amberson, and Mr. Banks, without whose careful dissection and cooperation the report of this case would not have been possible.

Attention was first drawn to the lymphatic system by finding, during the dissection of the lower neck and axilla, a number of lymphatic vessels which were unusually distended by a whitish coagulum. One of these vessels, larger than the others, extended down into the axilla, where it received branches from numerous enlarged lymph glands. The duct extended beyond the axillary glands, in the direction of the thoraco-epigastric vein, in the subcutaneous tissue of the lateral body wall. At about the level of the sixth intercostal space the duct was cut across, in separating the fascia at the dividing line between the two dissection fields, before it had been found that there was anything unusual about the lymphatics. At the cut end the diameter was still considerable, and it was remarked at the time that this vessel was very much larger than could be accounted for by the lymph coming from the axillary glands alone. Anteriorly the duct joins the left subclavian vein in the angle formed by this vein with the internal jugular. Near the opening a second, smaller lymph duct was found, joining the subclavian. A search was made before the thorax was opened for the terminal portion of the thoracic duct and a fine vessel was seen in the usual position for the end of the thoracic duct, but was broken during the dissection.

Somewhat later, Mr. Amberson, dissecting the lower left thoracic and abdominal wall, traced a supposed subcutaneous "vein" from the lateral thoracic region posteriorly over the abdominal wall, and over the ligamentum inguinale (Poupart's) into the superficial fascia of the femoral triangle. To his great surprise he found that ducts led from the inguinal lymph glands into this supposed "vein" — that, instead of a vein, he had been following a greatly enlarged lymph duct. The case now became one of much interest; from the size of the duct it was suspected that it must drain at least a part of the abdominal viscera. Fortunately the thoracic and abdominal viscera had not yet been disturbed, so that it was possible to dissect here the main lymphatics.

The duct which had been followed along the lateral thoracic and abdominal wall was first studied. (Fig. 2, m. l. d.) It is a substantial vessel, which is duplicated posteriorly and anteriorly by smaller vessels. The middle undivided part consists of a stretch, 10 cm. long, starting from a point 14 cm. from the ligamentum inguinale, where it receives the posterior duplicating vessel. (Fig. 2, p. d. l.) The main duct has a marked widening above the ligamentum inguinale. Below the ligament its diameter is about 2.2 mm., while 3 cm. above the ligament its diameter is approximately 4.0 mm. This diameter diminishes very gradually until, at a point 22 cm. from the ligament, it is reduced to approximately 2.0 mm. The main continuation anteriorly maintains this diameter of 2.0 mm., while the anterior duplicating vessel is about half as large. The cervical portion of the duct again widens until, at a distance of 3 cm. from its junction with the subclavian vein, it has a diameter of approximately 4.0 mm. The terminal portion, for about 1.0 cm., is distended with blood. The origin of the posterior duplicating vessel was not determined, as it was broken off during dissection. From the angle at which it joins the main vessel, and from the fact that, like the main vessel, it has a decided widening to 3.5 mm. at a corresponding place, there is little doubt that it took origin from lymphatic vessels in the inguinal region. All of the vessels were opened, in order to study the valves. In the main duct there is a valve, 1 cm. posterior to the ligamentum inguinale, a second valve 11.5 cm. anterior to the ligament, and a third above the point where the anterior duplicating vessel is given off. All the valves have the flaps directed so as to permit the lymph to run in an anterior direction. Between these three valves the inner wall of the duct is smooth. In the posterior duplicating vessel there are two competent valves, one in the widened region a short distance anterior to the ligamentum inguinale, and the second shortly below its junction with the main duct. The flaps of the valves are directed anteriorly. In addition there are numerous transverse thickenings which project into the lumen. In the anterior duplicating vessel a valve is present shortly beyond its origin from the main duct, its flaps directed anteriorly.

Unfortunately direct connection between the duct found in the body wall and the upper part, leading through the axilla to the subclavian vein, was, as has been explained, not seen. But, in view of the condition of the visceral lymphatics, to be described, there can be little doubt that they were continuous.

On dissecting the thoracic and abdominal viscera the following conditions are found: In the mid-thoracic region a miniature thoracic duct is present in its usual position between the azygos vein and the aorta. (Figs. 2 and 3, th. d.) At no part of its course does its diameter exceed three-fourths of a millimeter. On being followed anteriorly it is found to pursue the usual course, crossing to the left and coursing toward the junction of jugular and sub- clavian veins. As already noted, the connection with the vein was lost early in the dissec- tion. Posteriorly it grows smaller, and at the ninth thoracic vertebra it comes to an end by curving sharply to the right behind the azygos vein and by passing out into the ninth intercostal space in company with the ninth intercostal artery and vein. No trace what- ever could be found of a continuation further posteriorly of this miniature duct. Two or three minute tributaries were found joining the duct along its course. Careful dissection ventral, dorsal, and to the left of the aorta failed to reveal a possible left thoracic duct- As to the condition of the deep veins, the azygos vein presents a marked abnormality. First, it should be noted that the azygos and aorta lie rather further to the left than usual, so that the azygos, in the mid-thoracic region, is situated nearly in the midline. The usual one or more tributaries which cross the midline, dorsal to the aorta in the mid-thoracic region, carrying the blood from the hemiazygos, are absent. Instead, the left intercostal spaces, beginning with the fourth, are drained by veins collecting in a common trunk which runs posteriorly as far as the body of the ninth vertebra. This trunk is joined by a vein which runs from the left renal vein (fig. 3, a. l. v.), and receives the upper lumbar and lower intercostal branches. This vein represents a much widened ascending lumbar vein, continuous with the lower part of the hemiazygos vein. The common branch formed by these two veins is a trunk of considerable size, about 5.5 mm. in diameter, which crosses the midline ventral to the aorta, at the level of the ninth intervertebral disk, to become the chief tributary of the azygos. (Fig. 3, conn, v.) In fact, this branch is larger than the posterior continuation of the azygos itself, which is about 4 mm. in diameter. The azygos narrows rapidly below the point of junction of this branch, receiving branches from the tenth and eleventh intercostal and the subcostal spaces. A narrow vessel runs from the end of the azygos, across the body of the twelfth vertebra, dorsal to the aorta, and anastomoses with one of the left subcostal veins.

The vein mentioned, which runs from the left renal vein to join the left azygos, courses on the bodies of the vertebrae to the left of the aorta, and dorsal to the left renal arteries. It has a minimum diameter of about 2.7 mm.

Associated with this variation in the azygos veins is one of the left renal vein. This, instead of crossing the midline to the inferior vena cava, runs posteriorly, joining the vena cava at its origin opposite the angle formed by the two iliac veins. In addition to its connection with the inferior portion of the hemiazygos, the renal receives, as usual, the adrenal and ovarian veins. 1 The right renal vein is not abnormal.

To return to the lymphatics, it may be said at once that the abdominal and pelvic viscera, the intercostal spaces posterior to the ninth, and both posterior extremities are drained by lymphatics which collect into the left subcutaneous duct already described. (Figs. 2 and 3.) Following this duct backwards, it is found that, after passing superficial to the ligamentum inguinale, it runs posteriorly as far as the junction of the great saphenous vein with the femoral vein. It winds around the saphenous, as this vein passes through the deep fascia to join the femoral, and starts anteriorly along with the deep vessels. It soon divides, smaller branches passing superficial to the external iliac vessels, and running to the iliac lymph nodes which surround the external iliac vessels. The largest branch passes anteriorly at first medial to the external iliac vessels. A little above the ligamentum inguinale it winds around behind (dorsal to) the iliac vessels, until it lies lateral to the anterior third of the common iliac artery and vein. Here it divides into several branches, which pass in part to the more anterior iliac lymph nodes, in part anteriorly along the left of the aorta to the left lumbar nodes, and in part ventral to the aorta to drain directly the plexus surrounding the superior mesenteric artery and celiac axis.

The lymphatics, draining the abdominal and pelvic viscera and legs, reach the duct as follows: Several ducts from the left inguinal nodes join the main duct and its branches both before and after it curves around the saphenous vein. Others pass under the ligamen- tum inguinale to the lowest external iliac nodes. The lymph from the right leg, after pass- ing through the right iliac nodes, is carried by a number of ducts, some of which run across the front of the sacrum and the last lumbar vertebra to the left iliac nodes, while others pass anteriorly on all sides of the iliac vessels, the lateral ones running to the right lumbar nodes, the ventral and medial ones running in part to a large node which lies ventral to the aorta just before its division, whose efferents pass to the left iliac nodes and in part dorsal to the aorta and vena cava, curving to the left and entering the left inferior lumbar nodes and the anterior iliac nodes. From the pelvic viscera ducts pass to the right and left iliac nodes, the right nodes being drained by the ducts already described.

The abdominal lymphatics present an interesting condition. There is no definite receptaculum chyli, nor are there any especially widened vessels in the region where the receptaculum is usually found. Instead there are plexuses and numerous narrow vessels lying dorsal to the aorta and vena cava inferior on the bodies of the last thoracic and all

It should, perhaps, be noted that a double ureter is present on the left side; the left kidney is considerably longer. slightly narrower, but nearly twice as thick as the right, so that as a whole it is decidedly larger than the right. four lumbar vertebrae. 1 The most anterior of these reaches the body of the eleventh thoracic vertebra. The widest of these vessels is but 2 mm. For the most part they are vessels running from the right lumbar nodes across to the left side, to the left lumbar nodes, or to ducts which pass directly to the left iliac nodes. Some ducts from the plexus, opposite the last thoracic and first lumbar vertebrae, however, wind around the left of the aorta and reach the plexus around the celiac axis and superior mesenteric, which drain the intestines, stomach, and in part the liver. It is quite probable, therefore, that some of the lymph from these organs passed through the plexus which lies in the position of the receptaculum chyli.

The most anterior part of these lymphatic plexuses consists of a loop which passes from the right lumbar chain, anteriorly, as far as the division of the azygos vein. (Figs. 2 and 3, a.) Here, ventral to the azygos, it bends sharply to the left, and, running posteriorly, ventral to the aorta, passes to a gland lying to the left of the aorta, opposite the twelfth thoracic vertebra. It is to be noted that this loop reaches nearly to the level at which the rudimentary thoracic duct ends. The two are here separated by the anomalous azygos connecting branch (fig. 3, conn, v.), which is crossing from left to right, ventral to the aorta. No trace of a connection could be found between the two lymphatics by the most careful dissection.

Ventral to the aorta there are, in addition to the large lymph node over the bifurcation, two long, flattened nodes lying posterior to the place of origin of the renal arteries (fig. 3). These two nodes are connected with the node over the bifurcation by several vessels running along the aorta. They receive, also, vessels which course across the inferior vena cava, a vessel of considerable size which follows the vena cava as far as the diaphragm, vessels from the plexus around the celiac axis and superior mesenteric artery, vessels from the duodenal region and from the right lumbar glands. The two glands are connected with one another by several vessels. From the left of these two preaortic glands there is a glandular projection which passes dorsally to one of the left lumbar glands. From the left gland two vessels of considerable size run posteriorly, to the left lumbar and left iliac glands.

The vessels connecting the right lumbar chain of nodes with one another are less numerous than the corresponding vessels on the left side. Vessels were traced from the right chain to the tenth and eleventh intercostal spaces. On the left side, small vessels were found from the tenth and eleventh intercostal spaces which led to ducts passing pos- teriorly to the left lumbar nodes. A curious condition was found in the z'egion of the twelfth rib. A lymphatic loop distended with a whitish coagulum lies to the left of the body of the eleventh vertebra and on the neck of the twelfth rib. It is connected with a con- siderable lymphatic plexus lying to the left of the aorta, which, in turn, is connected with the plexus around the superior mesenteric artery and celiac axis. To the left of the aorta there is a group of lymph ducts, in part interrupted by the left lumbar nodes and in part running free of them, which starts anteriorly with the vessels mentioned draining the tenth and eleventh intercostal spaces, and extends to the iliac nodes. This group receives most of the vessels lying on the bodies of the vertebrae, the left renal and left ovarian lymphatics, and most of the vessels hying ventral to the aorta, including connections with the lymphatics from the intestines, liver, and stomach, which follow the celiac axis and superior mesenteric artery. Some of the ducts pass dorsal and some ventral to the renal arteries. In this region they form a plexus which is interwoven with the plexus of sympathetic nerves. Small vessels from this chain were traced to the pillars of the diaphragm, presumably draining some of the diaphragmatic lymphatics. From the inferior end of the left lumbar nodes a stream of ducts leads to the left iliac nodes. The large node already referred to, which lies ventral to the aorta near its bifurcation, receives (in addition to the vessels mentioned) ducts from the vessels accompanying the inferior mesenteric artery.

  • Only four lumbar vertebra; are present in this subject.

In brief, then, the conditions present are these: The thoracic duct is rudimentary; it occupies its normal position, but extends posteriorly only as far as the body of the ninth vertebra, where it starts as a small vessel draining the ninth intercostal space. The dorsal body wall posterior to the ninth intercostal space, the abdominal and pelvic viscera, and both posterior extremities are drained by vessels which collect into a large duct which starts in the region of the anterior iliac lymph nodes opposite the last lumbar vertebra, runs pos- teriorly beneath the ligamentum inguinale, hooks around the terminal bend of the great saphenous vein, and then courses anteriorly in the superficial fascia over the ligamentum inguinale, over the lateral abdominal and thoracic wall, through the axilla, and into the left subclavian vein near its juncture with the internal jugular.

Associated with this condition is a variation of the hemiazygos and left renal veins, significant features of which are: (1) the veins draining the left intercostal spaces, below the third, collect into a vein which crosses to the right ventral to the aorta, at the level of the ninth thoracic vertebra, to join the main azygos, and this cross branch lies between the lower end of the thoracic duct and the most anterior loop of the abdominal lymphatics; (2) there is a considerable anastomosis between the hemiazygos and the left renal which, in turn, runs posteriorly to join the inferior vena cava at its point of formation by the junction of the two iliac veins.

So far as I have been able to learn, no such abnormality of the lymphatic system has been described.

While any explanation of this condition must necessarily be mainly speculative, certain facts, in connection with our knowledge of the mode of development of lymphatics, are suggestive. First, it should be noted that there is no evidence of any pathological condi- tion in the region where the thoracic duct ends. Turning then to the embryo, it has been shown by Miss Sabin (1, 1913, 63) that, in pig embryos, valves begin to develop in lym- phatic vessels in embryos of 7 cm. Thus, she was able, in embryos of 5.5 cm. (2, 1904, 86), by inserting the injecting needle into the dermis at any point, to inject the entire network of subcutaneous lymphatics, which form, at this stage, a richly anastomosing network over the body wall. In human embryos Miss Sabin (3, 1912, 728) found that valves apparently begin to develop in the larger vessels of the subcutaneous network in embryos of 5.5 cm. For a considerable time previous to the development of valves, the body-wall plexus collects anteriorly into ducts which pass into the axillary region, posteriorly into ducts which pass into the depth in the inguinal region, and which eventually reach the recep- taculum. Polinski (4, 1910) has demonstrated, in bovine embryos, a temporary lateral vessel which differentiates in the midst of the plexus in the lateral body wall. Mierzejewski (5, 1909) has found in chick embryos a transitory longitudinal vessel in the body wall which runs from the axilla along the lateral body wall over the pelvic region. Mrs. E. L. Clark, in a series of observations, soon to be published, and which she kindly permits me to refer to, on the circulatory conditions in the superficial lymphatics of living chicks, finds that the circulation in lymphatics starts very gradually and that, in early stages, slight disturbances may result in a complete reversal of the direction of lymph flow. Obviously, then, since there is a considerable period in which no valves are present, there is the possibility that were there any unusual condition which should offer a sufficient resistance to the flow of lymph through the thoracic duct, the lymph might make its way posteriorly in the deep abdominal lymphatics, and, passing through the inguinal lymphatics to the super- ficial body wall, eventually reach the subclavian vein by way of the axilla. In the present case such an obstruction may well have been afforded by the anomalous condition of the azygos vein, for the line of division between the rudimentary thoracic duct and the lym- phatics draining posteriorly occurs at exactly the place where the large connecting branch from the veins draining the left thoracic cavity crosses in front of the aorta. While this vessel appears relatively small in the adult, much too small, perhaps, to be considered sufficient to cause an obstruction to the flow of lymph, it should be remembered that in young embryos the veins are relatively enormous. Moreover, since the left renal vein runs posteriorly to the junction of the two iliacs, and since there is still a connecting vein of considerable size from the left renal to the lower branch of the left azygos, it is highly probable that for a considerable embryonic period this vein carried much of the blood from the left leg, left half of the pelvis, left kidney, and left lumbar region.

Fig. 1. Transverse section through the region of the seventh thoracic vertebra of an injected human embryo (Carnegie Institution of Washington, Embryological Research, Collection No. 460, 21 mm. long, slide 26, row 1, section 4). The section passes through one of the anastomoses between the hemiazygos and azygos veins, passing, as it does normally, dorsal to the aorta. There is a lymphatic vessel on each side of the aorta, ven- tral to the azygos and hemiazygos veins respect- ively. The lymphatic on the right becomes normally the thoracic duet. Enlarged 38X- Drawn with camera lueida.

t. A., Intercostal artery.

7 t. v., Seventh thoracic vertebra.

a. v., Azygos vein.

T. D., Thoracic duct.

a., Aorta.

K. L., Right lung.

o., Esophagus.

i. v. c, Inferior vena cava.

H. v., Hemiazygos vein.

l., Lymphatic.

There is another possibility which should be mentioned: While the exact mode of development of the thoracic duct is not entirely settled, it is probable, as Miss Sabin (1, 1913) has suggested, that the anterior part is formed by the growth (in a posterior direction) of rudiments which have budded off from the veins in the neck, and that the posterior part is formed by the growth (in an anterior direction) of rudiments which bud off from the renal veins; that the two sets meet and anastomose, and eventually form the continuous thoracic duct. If such is the case, it is possible that the anomalous azygos branch has prevented the union of the two sets.

The actual conditions which are present in the normal human embryo are shown in figure 1 , which represents a cross-section through the region of the seventh thoracic vertebra in an injected human embryo (No. 4G0, 21 mm., in the collection of the Carnegie Institu- tion of Washington). The section shows the two azygos veins connected by a cross-anas- tomosis passing dorsal to the aorta. The relatively large size of the embryonic veins is obvious. In the angle between each azygos vein and the aorta there is a lymphatic vessel, the one on the right side being the early thoracic duct. It is easy to imagine the obstruc- tion to the growth of lymphatics, which would be present, were the connection between the two veins ventral instead of dorsal to the aorta, especially in case the left vein and the connecting branch were much larger than in the section shown. Such a condition must have obtained in early embryonic stages in the case under discussion.

This case furnishes a most striking instance of the dependence of anatomical structure on mechanical factors. Out of the lymphatics of the subcutaneous tissue of the left body- wall, which ordinarily develop into narrow vessels draining in two directions, into the axilla and the inguinal region, with capillary or (at most) very narrow anastomosis, there has been produced a large vessel through which passed all the lymph of the posterior half of the body, while the thoracic duct, deprived of this drainage, is a minute vessel, hardly more than one- tenth its normal size, extending posteriorly only as far as the ninth thoracic vertebra. More- over, along the course of this subcutaneous duct, anterior to the ligamentum inguinale, there is a definite widening, corresponding somewhat to the receptaculum chyli, which is missing. That blood-vessels are governed in their growth by mechanical factors has been shown by Thoma (6, 1893) who finds that an increase or decrease in the amount of blood-flow leads to increase or decrease in the size of the vessel, while an increase or decrease in pressure causes increase or decrease in the thickness of the wall. It is apparent that lymphatic vessels respond similarly to mechanical forces, since the passage of a large amount of lymph through an unusual route has led to the formation of a duct many times larger than the vessels normally present, while the diminution in lymph flow through the thoracic duct has been accompanied by a corresponding diminution in its size.


1. F. R. Sabin. 1913. The origin and development of the lymphatic system. The Johns Hopkins Hospital Monographs, New Series, No. 5, 1913.

2. F. R. Sabin. 1904. On the development of the superficial lymphatics in the skin of the pig. American Journal of Anatomy, vol. I.., 1904, p. 193.

3. F. R. Sabin. 1912. Development of the lymphatic system. In Manual of Human Embryology, by Keibel and Mall, vol. n. 1912. 1893.

4. W. Polinski. 1910. Untersuchungen iiber die Entwieklung der subcutanen Lymphgefasse der Siiuger, inports. Sonderheit des Rindes. Extrait du Bulletin de la e deS Sciences d « Cracovie, 1910 ' £ 313

5 " L T Mierzejewski. 1909 Beitrag zur Entwieklung , lea Lymphgefasse-systems der Vogel. Extnut du Bulletin de 1 Acadenue des Sciences de ( racovie, 1909, p. 4/ 'J.

6. R. Thoma. 1893. Untersuchungen iiber die Histogenese und HistomechanikdesGefasssvstems. Stuttgart,

Explanation of Figures 2 and 3

Fig. 2. Drawing to show the deep abdominal lymphatics, the thoracic duct, and the subcutaneous duct in the case described in the text. The inferior half of the aorta and the inferior vena cava are removed to show the plexus and glands lying on the bodies of the vertebrae. The azygos vein is cut and drawn back to show the ending of the minia- ture thoracic duct. The * shows the place at which the subcutaneous duct was divided early in the dissection. The anterior end of the left kidney is cut off to show underlying lymphatics. The arrows are opposite the place where definite valves were found in the subcutaneous ducts. A, most anterior of lymphatics of abdominal plexus; a. d. l., anterior duplicating lymphatic; m. l. d., main lymph duct; p. d. l., posterior duplicating lymphatic; th. d., thoracic duct, ending blindly anteriorly, where it was broken during dissection; v. saph. m., vena saphena magna. In the lumbar region several cut ends are shown of vessels which passed ventral to aorta and vena cava; the continuations of these vessels are shown in fig. 3.

Fig. 3. Drawing to show the abdominal lymphatics lying ventral to aorta and vena cava inferior. Their connections with the deeper lymphatics are shown as cut ends. The arrow indicates the beginning of the main lymphatic dud a, same as fig. 2; a. l. v., ascending lumbar vein, running from the renal vein to join with the hemiazygos vein (hemiaz. v.) to form the connecting vein (conn, v.), which crosses ventral to the aorta to join the azygos vein; L. hen. v., left renal vein; l. ov. ves. and r. ov. ves., left and right ovarian vessels; ccsl. ax., celiac axis; sup. mes. a., superior mes- enteric artery; inf. mes. a., inferior mesenteric artery; th. n., thoracic duct.

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