Book - Contributions to Embryology Carnegie Institution No.58
CONTRIBUTIONS TO EMBRYOLOGY, No. 58.
ON THE FATE OF THE PRIMARY LYMPH-SACS IN THE ABDOMINAL REGION OF THE PIG, AND THE DEVELOPMENT OF LYMPH- CHANNELS IN THE ABDOMINAL AND PELVIC REGIONS,
BY F. L. REICHERT.
With five text-figures.
Since 1900 interest in lymphatics has been centered about the question of their origin and development. The primary lymph-sacs have been worked out and in general their fate determined. Sabin (1901-2) has shown that the earliest lymphatic buds arise in association with the anterior cardinal veins and form the primary lymphatics in the neck the paired jugular sacs. The other primary sacs originate indirectly from the vena cava through the veins of the Wolffian body. These are the paired iliac sacs, the cisterna chyli (Sabin, 1912) and the retroperitoneal sac (Lewis, 1906; Baetjer, 1908). Quoting from Sabin (1913):
"In most general terms the jugular sacs drain the anterior half of the body; the iliac sacs drain the posterior half of the body; while the retroperitoneal or prse-aortic sac drains the viscera. The cisterna chyli with the thoracic duct connects the jugular and renal lymphatics."
The recent work on the origin of blood-vessels by the differentiation of angio- blasts, or vaso-formative cells from mesenchymal cells (Stockard, 1915; Sabin, 1920; Streeter, 1920), may result in modifying our present conception of the origin of the lymphatics to some such form 'as this: that they arise either directly from the endo- thelium of the veins or in part by a differentiation of new cells analogous to angio- blasts. The experiments of E. R. and E. L. Clark (1920) point in that direction. It is clear, however, that lymphatics begin centrally, close to certain veins, and spread peripherally.
Considering the sequence in the development of the primary lymphatic system, it was at first thought by Sabin (1901) that the earliest lymphatics in the pig were sacs which bud off from certain veins. F. T. Lewis (1906), going back a step farther, showed that in the rabbit the formation of the primary lymph-sacs is preceded by a plexus of blood-filled capillaries connected with the veins. This was confirmed by Sabin (1912) for pig and human embryos, and by Huntington and McClure (1910) for the cat. Recently E. R, and E. L. Clark (1920) have carried the investigation back still farther in the chick, practically to the beginning, when the first evidence of lymphatics consists of a few blood-filled vessels lined with characteristic lymphatic endothelium and connected with veins. These vessels later join to form a circumscribed continuous plexus of vessels which does not have a continuous lumen and which is still connected with the venous system in a number of places. This plexus is the primordium of the lymph-sacs or lymph-hearts, from which the lymphatics of the body arise and grow peripherally. As stated by Sabin (1913), these buds in connection with veins form "a new type of vessels, namely, lymphatics. These buds unite to form plexuses which develop into sacs. These sacs may become lymph-hearts. From these lymph-sacs or hearts lymphatic capillaries gradually invade the body in orderly sequence in definite and character- istic zones and layers. The growth is always in the capillary bed that is, all lymphatics develop as capillaries, and the earliest ones to develop become the first lymph trunks or ducts." To make the story more complete (at least in the pig), in the next stage these lymph-sacs break up and are converted into a coarse plexus of lymph-channels, which in turn are transformed into lymph-nodes or glands.
As to the secondary lymphatic system that is, the peripheral vessels the development of those of the skin (Sabin, 1904), small intestine (Heuer, 1909), lung (Cunningham, 1916), heart and stomach (Cash, 1917, 1921) has already been studied.
The work of A. H. Clark (1912-13) on the fate of the jugular lymph-sacs gives a general survey of the lymphatics of the anterior region of the body in the pig and shows how the lymphatic channels of the head, neck, and thorax are related to the primary lymph-glands. In the present paper it is desired to give a similar survey of the lymphatics in the abdominal and pelvic regions and to determine more definitely the fate of the primary sacs of the abdominal region. No attempt will be made to present in detail the development of the lymphatics of the different organs.
Throughout the investigation the encouragement and assistance of Dr. Florence R. Sabin have been a constant help, and my sincere appreciation and thanks are due to her.
The material consisted of living pig embryos varying in length from 4 to 20 cm. The lymphatics were injected and the specimens cleared by the Spalteholz method as described by Sabin (1915). Silver nitrate (2 per cent) and india-ink were used for injections. With the latter the injections were nearly complete. Some were made through the retroperitoneal sac, but more thorough injections of the abdominal and pelvic regions were secured by introducing the needle into the thoracic duct on the left side, a short distance posterior to and behind the arch of the aorta, as described by Heuer (1909).
At about the stage of 7 cm., valves are being formed in the lymphatic vessels and the primary sacs no longer remain homogeneous, but begin to break up into plexuses of vessels which are the forerunners of the primary lymph-glands. For this reason, beyond the stage of 8 cm., when it was difficult to get the injection mass to pass the valves, the different organs were injected directly and the lymphatic drainage to the several glands was thus indicated.
In the pig the origin of the lymphatics of the abdominal and pelvic regions can be traced to lymphatics arising ventral to the aorta (fig. 1) and dorso-lateral to the aorta (fig. 4). With the growth of the embryo and the beginning formation of the lymph-glands this distinction can not be made out so readily, since in both cases the glands tend to lie lateral to the aorta. When glands are definitely formed, those arising from lymphatics dorso-lateral to the aorta in the main lie with those from the ventral side.
LYMPHATICS ARISING VENTRAL TO THE AORTA.
In the smaller embryos, beginning at about 23 mm., there is a primary lym- phatic sac the mesenteric (Lewis, 1906) or retroperitoneal sac, as it was termed later (Baetjer, 1908) situated outside of the peritoneal cavity. This sac lies between the paired Wolffian bodies and gonads, just ventral to the point of renal anastomosis of the subcardinal veins, and extends from the region of the superior mesenteric artery to a point near the bifurcation of the aorta (fig. 1). Up to about 7 to 8 cm. it is a complete sac spreading sheet-like between the Wolffian bodies (Heuer, 1909, figs. 3 and 4), and later between the kidneys.
Lewis (1906) describes the sac in rabbit embryos of 21 mm. as situated at the root of the mesentery, just ventral to the point of renal anastomosis of the sub- cardinal veins. Baetjer (1908) has shown that it has its origin in numerous venous capillaries which, by increase in number and by fusion, form a sac which has definite connections with the subcardinal veins. There follows a gradual obliteration of these venous connections and for a short period the sac is an isolated structure with irregular margins. By the stage of 25 mm. it has gradually developed connections with the rest of the lymphatic system by an upgrowth of small lymphatic capillaries along the margin of the aorta. Heuer (1909) describes three main connections with the lymphatics dorsal to the aorta :
(1) There are several afferent vessels which arise from the mesial trunk as it leaves the anterior end of the sac and course ventro-dorsad and slightly anterior to enter the thoracic duct (fig. 2, Anas. ant.).
(2) The main efferent connection is a stout trunk (fig. 2, Anas, maj.) opposite the anterior pole of the kidney, between the cisterna chyli and the anterior end of the sac.
(3) A third connection is made from its posterior portion to the caudal part or fan of the iliac sacs. Also, along the renal portion of the aorta there are numerous anastomoses with the lymphatics dorso-lateral to the aorta.
Anterior portion of sac. This large sac ventral to the aorta may be divided in the region of the hilum of the kidney into an anterior and a posterior portion (fig. 1). The anterior portion gives rise to two main trunks, the large anterior or coeliac trunk and the small posterior or superior mesenteric trunk. Figure 1 shows the ventral or retroperitoneal sac in a pig embryo 7.8 cm., after it had begun to split into a plexus of lymphatic vessels, the forerunners of its transformation into lymph-glands. In the pig it is at this stage a very extensive plexus, in contrast with its earlier sac-like form (Heuer's fig. 4), and its main portions are seen to lie on either side of the aorta, where they form a coarse network of channels. It will be noted that the fold of mesentery and the cceliac trunk have been cut and the stomach turned aside to expose the lymphatics from the anterior end of the sac. At this stage the kidneys have developed into large structures and the Wolffian bodies have begun to degenerate and are pushed to the side. The artist has clearly shown the relationship of the various parts of the reproductive system.
The large coeliac trunk (figs. 1 and 2, T. coel.) immediately divides into a right and a left branch, the latter soon breaking into the mesial trunk and the left trunk. The left trunk, which includes the gastro-splenic trunk, is not shown in figure 1, being on the other side of the fold of mesentery, but it can be well seen in figure 3. The mass of lymphatics at the anterior end of the retroperitoneal sac courses cephalad for a short distance and then turns ventrally, breaking up into several main lymphatic branches. This ventral curve is shown in figure 2. A little way beyond the origin of the mesial trunk, lymphatic vessels pass laterally to spread (at
V I c vmin. V I
T. coel . Liq.diaph.
Flo. 1. Ventral view of pip em- bryo (No. 73) 7.8 cm. long, showing ventral or retroperi- toneal sac broken up into a coarse plexus, a stage about midway between the earlier complete sac and later group of lymph-glands. Lymphat- ics injected with india-ink ' through the thoracic duct. ' Drawing made from speci men by J. F. Didusch.
Liq Geniroinq. Or. uret. in urog.
first in the form of a film, but in older embryos as distinct vessels) over the adrenal capsule and the anterior pole of the kidney (fig. 3, V. 1. cap. gl. suprar.). As the trunk twines ventrally around the body of the pancreas, lymphatics are given off to the middle portion of that organ. These pancreatic vessels are not shown in figure 3, but would come off in front of the lower portion of the trunk of the lesser curvature (T. c. V. min.). Laterally, vessels pass from the mesial trunk to the diaphragm (fig. 1, V. 1. diaph.), uniting with those from the anterior end of the iliac sacs.
From the mesial trunk, as previously stated, there are several efferent vessels emptying into the thoracic duct (fig. 2, Anas, ant.) On either side of these vessels several long lymphatic channels run cephalad with the pulmonary ligament to supply the lower portions of the lung (fig. 2, V. 1. pulm.). The largest trunk of the
V I me 3
Ramus Retroren.. S.il.
5. il.pors caud.
FIG. 2. Right lateral view of pig em- bryo (No. 24) 6 cm. long, showing connections and relative positions of the primary lymph-sacs that is, of the retroperitoneal sao and the iliac sacs. Lymphatics in- jected with india-ink through the thoracic duct. Drawing made from specimen by J. F. Didusch.
_Vena omph mea, A umb.
mesial mass is the gastric trunk of the lesser curvature, which is described by Cash (1921). This is shown in part in figure 1, but still better in figure 3, which is a view of the stomach from below, designed to show the main mass of lymphatics of the lesser and greater curvatures and special lymphatics of the pylorus. It shows also the relation of the lymphatics to the pancreas. It is to be noted that the spleen, with the lymphatic vessels in its capsule and mesentery, has been removed and that the gastro-splenic trunk has been cut just as it is dividing into its two terminal branches. The intestines have been removed, leaving only the stump of the superior mesenteric trunk. This gastric trunk terminates at the lesser curvature by dividing into two branches: (1) an ascending or left branch, which supplies the cardiac region of the stomach, forms a network of periesophageal lymphatics, and sends out vessels to the medial portion of the diaphragm; (2) a descending or right branch, which likewise supplies the cardiac region, diaphragm and lesser curvature (fig. 2, V. 1. diaph.; T. c. v. min.), and anastomoses with other vessels supplying the diaphragm and lesser curvature.
The left trunk, of which the main branch is the gastro-splenic trunk (fig. 3), passes ventrally to the fundus of the stomach. Near its origin it sends lymphatics to the tail of the pancreas. It continues on to the fundus as the gastro-splenic trunk, then divides beneath the posterior third of the spleen, one branch immediately breaking up to supply the region of the fundus, the other coursing along the length of the spleen in its ligament to a point near the pyloric extremity. Here it again divides, the smaller branch to continue to the pole of the spleen, the larger turning obliquely toward the greater curvature of the stomach, where it forms a T-shaped termination (fig. 3, V. 1. c. v. maj.) One limb passes toward the cardiac pouch, breaking into many small vessels on the curvature and finally anastomosing with the vessels supplying the fundus; the other limb passes toward the pylorus and likewise drains the greater curvature and anastomoses with the lymphatics of the pylorus. These anastomoses are well shown in figure 3. In none of the specimens could an injection be secured which involved the parenchyma of the spleen itself.
V.I. corp. pan.
T.qast.dexf V. I. asc. duo
Fio. 3. Pig embryo (No. 74), 6 cm. long. Ventral view of anterior end of retroperitoneal sac, showing the main gastric trunks and the lymphatics of the pancreas. The spleen has been removed. Lymphatics injected with india-ink through the thoracic duct. Drawing made from specimen by J. F. Didusch.
The right branch arises from the right half of the cceliac trunk and courses ventro-laterally along the gastro-pancreatic line with the hepatic artery, breaking into two branches the hepatic vessels and the right gastric trunk (fig. 3, T. gast. dex.). From the right gastric trunk the pyloric vessels (fig. 3, V. 1. pyl.) pass along the pancreas to the pyloro-duodenal junction, where they turn abruptly forward over the pylorus to anastomose with the lymphatics of the greater curvature . This trunk also sends lymphatics to the body of the pancreas (fig. 3, V. 1. corp. pan.).
There are two sets of lymphatics going to the liver. The main mass passes along with the hepatic artery, going behind the pyloric end of the stomach (figs. 1, 2, and 3; V. 1. hep.). These vessels unite with the other lymphatics accompany- ing the biliary ducts to form the hepatic trunk (fig. 2, V. 1. hep.) . These lymphatics course along with the blood-vessels within the liver in the perivascular and peri- lobular tissue, but not to the lobule of the organ itself (Mall, 1901). The second hepatic set or trunk arises just posterior to the large anterior or cceliac trunk. This lateral trunk splits off laterally from the right side of the retroperitoneal sac toward the portal vein, which it accompanies for a short distance, then branches at right angles, sending vessels in both directions along that vein. Those passing posteriorly unite with those going to the head of the pancreas. As they approach the liver, these vessels along the portal vein join with those of the hepatic branch from the cceliac trunk to enter at the hilum of the liver, although some accompany the biliary ducts and go to the gall-bladder.
The other main ventral branch from the anterior end of the retroperitoneal sac is the small posterior or superior mesenteric trunk, the stump of which is shown in figure 3. This trunk arises from the sac at about the origin of the superior mesenteric artery and its branches become the satellites of the branches of that artery in the mesentery (fig. 2, V. 1. mes.). The trunk appears in figure 2, which is a view of the lymphatics from the side, and shows quite well the relation of the retroperitoneal sac to the iliac sacs, both as to position and connections. It also brings out the enor- mous mass of lymphatic vessels arising from the anterior end of the retroperitoneal sac. The trunk divides shortly, the smaller (duodenal) branch (figs. 2 and 3, V. 1. asc. duo.) supplying the lower portion of that section of the small intestine and anastomosing with the vessels from above. Lymphatics are also given off from this duodenal branch to the head of the pancreas (fig. 3). The other, the mesenteric branch (fig. 2, V. 1. mes.), is large and supplies the rest of the small intestine as well as the coils of the large intestine, the ascending, transverse, and descending colon.
Posterior portion of sac. Arbitrarily, the retroperitoneal sac was divided at the hilum of the kidney into an anterior and a posterior portion, but even at the anterior pole the sac is seen to broaden so that it occupies the interval between the mesial borders of the two organs. In earlier stages it extends to the hilum of the Wolffian body. In later stages (7 to 8 cm.) vessels from the lateral side of the sac enter the kidney at the hilum in company with other lymphatics from the dorso-lateral side of the aorta (fig. 1, V. 1. ren.) . In earlier stages, when the Wolffian bodies are large and completely hide the kidneys in a ventral view, the whole posterior lateral edge of the sac sends a sheet of parallel blunt processes, transverse to the axis of the embryo, which extend a short distance on both the dorsal and ventral capsules of the Wolffian bodies, as well as entering the mesial border in company with the blood-vessels of the glomeruli. At the stage shown in figure 1 the sac does not extend to the mesial border of the Wolffian body, but only a short distance over the ventral surface of the kidney, where numerous stout vessels accompanj' the meso- nephric veins. As these veins atrophy the satellitic lymph-vessels disappear. The remnants of the blunt processes are here shown passing obliquely backward to the posterior part of the Wolffian body and leading to a characteristic plexus along the medial ridge of the Wolffian body the gonadal plexus (fig. 1, V. 1. gon.). Thus, of the numerous blunt processes going to the Wolffian body, only those related to the gonads and other reproductive structures persist; the others disappear and this gonadal plexus becomes the genital branch, appearing in the stage shown in figure 1 as a fine plexus arising from the retroperitoneal sac at its lateral border, just cephalad to the bifurcation of the aorta, and passing laterally to the posterior medial end of the Wolffian body. Here part of the vessels turn sharply and course cephalad along the mesial border of that organ forming a fine plexus about the gonadal blood- vessels. This anterior branch continues to the hilum of the gonad which it supplies. The genital branch also forms a network over the caudal end of the Wolffian body, as well as giving off branches to the Mtillerian and Wolffian ducts and the gonadal ligament. In the earlier forms the sac sends lymphatics to the medial side of the umbilical cord, where they anastomose with those from the posterior portions of the iliac sacs. In the later stages they fail to inject.
Thus the peripheral spread of the lymphatic vessels from the posterior part of the retroperitoneal sac has been described; it remains only to mention the third efferent connection, which arises from the posterior end of the retroperitoneal sac, passes laterally to the outer side of the umbilicus, and then turns dorsally to join the caudal ends of the iliac sacs.
LYMPHATICS ARISING DORSO-LATERAL TO THE AORTA
Besides the paired anterior or jugular sacs there is another pair, the iliacs, which grow along the dorso-medial edge of the Wolffian body, dorso-lateral to the aorta, and drain the posterior half of the body. Figure 4 shows these two iliac sacs slightly dorso-lateral to the aorta and also their relation to the cisterna chyli and thoracic duct. It will be noted that there is an extensive plexus between the two sacs, while the paler vessels in the depth are from the retroperitoneal sac. The remnants of the Wolffian bodies show at the posterior borders of the kidneys. The iliacs are connected with the jugulars by the cisterna chyli and thoracic duct. Sabin (1912) has shown that the cisterna chyli and iliac sacs arise from the mesone- phric veins of the vena cava.
In the younger specimens, in the region of the diaphragm the thoracic duct is seen as two vessels, one on either side of the aorta, lying dorsally. These anasto- mose freely in front of and behind the aorta by lateral vessels. At about the same level as the anterior end of the retroperitoneal sac the vessels of the thoracic duct unite to form posteriorly an irregular dilatation, the cisterna chyli, extending to a point near the posterior poles of the kidneys.
From the lymphatics lying dorso-lateral to the whole length of the aorta that is, from the thoracic ducts, the cisterna chyli and the anastomosing iliac sacs- other lymphatics are given off dorsally as satellites of the segmental arteries which accompany the anterior and posterior rami. No vessels were observed, however, to enter the vertebral canal with the spinal branch of the posterior ramus, which is in accord with previous embryological studies, from which it was evident that the central nervous system contains no lymphatics.
Caudal to the cisterna chyli, and draining into it, are two large trunks, one on either side of the aorta. These are the paired iliac sacs, which in earlier stages appear to be united. Small at the cephalic end where they form the cisterna chyli, they broaden out gradually to form a rectangular sac between the dorso-medial surfaces of the kidneys and show two expansions. The lateral one is at the hilum of the kidney to which it sends vessels and a small trunk extending laterally in the body- wall to a retrorenal position, then turning abruptly caudad to unite with a trunk from the posterior portion (fig. 2, Ramus retroren.). In older embryos the latter gradually disappears. The other expansion occurs at the posterior end and may be called the caudal portion of the iliac sac. It is roughly fan-shaped, the expansion being latero-posterior, the outer margin curving with the posterior pole of the kidney (fig. 4, S. II. pars caud.).
In later stages, even at 5 cm., a distinct change is noted in the lymphatics dorso- lateral to the aorta (fig. 4). The iliac sacs are no longer fused, but come to lie on either side of the midline between the aorta and the medial edge of the kidney. They empty through one or two trunks into the cisterna chyli in the region of the adrenals. Their median border, accompanying the aorta, is straight and may sometimes, even in the earlier stages, send anastomosing vessels to the other side.
With the growth of the embryo these sacs come to lie entirely lateral to the aorta in approximation to and above the retroperitoneal sac, which likewise has become situated lateral to the aorta.
These three sacs are connected by small channels which show in figures 2 and 4, and when they are transformed into lymph-glands the result is a rather confusing
V I 3iaph
V. I. sacr. lot
FIG. 4. Dorsal view of specimen seen in figure 1, showing primary lymphatics dorsal and dorso- lateral to the aorta, namely, the thoracic duct, cisterna chyli, and the paired iliac sacs. Lymphatics injected with india-ink through the thoracic duct. Drawing from specimen by J. F. Didusch.
mass of right and left juxta-aortic lymph-nodes which is made up of glands aris- ing from lymphatics both dorsal and ventral to the aorta, and which extends from just above the hilum of the kidney to the bifurcation of the aorta, forming the main mass of lumbar nodes of the adult. Since the glands arise not only from the ventral and dorsal sacs, but probably also along some of the anastomosing vessels between these sacs, the resulting lymph-glands in the adult are exceedingly difficult to analyze in terms of dorsal and ventral lymphatics. However, there are glands arising from a small dorsal trunk or plexus which form the post-aortic or prevertebral nodes, but these are few in number (fig. 5, Lymgl. praevert.).
From the cephalic end of the iliac sacs lymphatics pass forward, anastomosing with those from the retroperitoneal sac to supply the diaphragm (fig. 4, V. 1. diaph.). The adrenals receive several vessels (V. 1. gl. suprar.) which arise from this cephalic end of the sacs in company with those which pass to the diaphragm. As mentioned previously, the kidney receives at its hilum vessels from the iliac sac (fig. 4, V. 1. ren.). There appears, therefore, to be a double supply to that organ, the vessels from the iliac sacs and those from the posterior half of the retroperitoneal sac. These vessels do not seem to penetrate very deeply into the kidney. Besfdes the vessels to the hilum of the kidney, a rather stout trunk, broad at the base, arises at this point and extends laterally in the dorsal wall. At times this is quite a large lateral expansion from the iliacs and forms a retrorenal sac which gives off one or more branches passing posteriorly at right angles to the body-wall, and anastomosing with similar vessels from the caudal end of the iliacs (fig. 2, Ramus retroren.) . It also sends a few vessels into the lateral body-wall, where a small plexus is formed which drains part of the deeper layers of the wall. Very few if any superficial vessels drain into it. As stated before, in older embryos these retrorenal branches could not be injected.
Caudal portion of sac. The fan-shaped caudal portion of each iliac sac lies in the body-wall between the posterior pole of the kidney and the bifurcation of the aorta (fig. 4) . It extends laterally and dips ventrally on its mesial side. Later it forms an inverted Y-shaped expansion, one branch passing laterally along the posterior pole of the kidney, the other going directly caudal and then turning ventrally to supply the lower portion of the body and legs.
From the lateral branch, in the earlier stages, a few vessels or a small trunk course cephalad to anastomose with the vessels from the retroperitoneal sac. Laterally, this caudal portion sends a group of lymphatics through the body-wall to form a superficial node just above the crest of the ilium (the ilio-inguinal node) which is characteristic for the pig, and drains the skin of the posterior half of the body and tail (Sabin, 1904). From the medial side of the posterior branch of the caudal portion one or two vessels pass caudally in the dorsal wall along with the lateral sacral vein (fig. 4, V. 1. sacr. lat.). On the postero-medial side of the sac a short trunk extends ventrally, medial to the umbilical artery, to anastomose with another trunk from the retroperitoneal sac.
The posterior trunk (fig. 4, T. post.), which drains the lymphatics of the legs and some of the pelvic organs, is the continuation of the medial branch of the caudal portion, which courses ventrally and laterally, passing lateral to the umbilical artery along the common iliac artery (fig. 1 , T. il. com.) . Only the proximal portion of the posterior trunk is shown in figure 4, for as it turned ventrally it became less and less distinct from the dorsal side of the embryo; but in figure 1, which is a ventral view of the same specimen, the continuation of the posterior trunk is well seen. It divides into several branches, two of which are proximal. From its medial edge, near its origin, the trunk sends a vessel ventro-medially to the lateral side of the umbilical cord, where it anastomoses with a similar vessel from the retroperi- toneal sac. It also sends lymphatics ventrally, in company with the vessel to the umbilical cord, to break up into smaller vessels over the posterior pole of the Wolffian body, where it evidently supplies part of the Mullerian and Wolffian ducts (shown on the left side of fig. 1) just at the inferior pole of the Wolffian body. This seems an important point, for, as will be noticed in figure 1, the lymphatics of the gonad itself are related primarily to one set the ventral lymphatics, derived from those of the Wolffian body while the lymphatics of the accessory genital organs are shown to be embryonically related to two sets of lymphatics those from the ventral or retroperitoneal sac, and those from the dorso-lateral or iliac sacs.
The posterior trunk then continues as a definite group of lymphatics, the com- mon iliac trunk following the artery of that name. It terminates by dividing into two smaller branches, the more important of which is the femoral or external iliac. These terminal vessels of the posterior trunk are satellites of the main arteries of the pelvis and hind-limb (fig. 1). In the stages at which the injections were made, the first or primitive arrangement of the blood-vessels of the posterior part of the body has changed, so that the blood comes from the aorta by way of the two common iliac vessels, which arise dorso-laterally just anterior to the origin of the umbilical arteries. Each passes caudally, lateral to the umbilical cord, sending a branch (the ilio-inguinal) around the pole of the kidney. At or just beyond the passage into the pelvic wall it divides into two main vessels. One of these, the internal iliac or hypogastric, which runs dorso-medially, divides into a number of terminal branches. The other, the femoral or external iliac, continues ventrally to the front of the hind- limb. At the proximal end of the femoral the now a trophic sciatic artery arises.
The common iliac lymphatic trunk broadens considerably at the bifurcation of the common iliac artery and then divides into a ventral and dorsal branch. The dorsal trunk the internal iliac or hypogastric (fig. 1, T. hypo.) accompanies the internal iliac artery and terminates by breaking into a number of vessels, satellites of the lesser arterial branches. A short distance from its origin the ventral branch the femoral or external iliac (T. il. ext.) sends a few lateral branches with the sciatic artery. It divides shortly, many of the vessels turning medially to form the inguinal trunk (fig. 1, V. 1. ing.) which drains a plexus of lymphatics along the inguinal ligament. This plexus is converted into two large elongated nodes, one situated more deeply than the other. These break up into a group of deep and super- ficial nodes which drain the lower abdominal wall, external genitalia, perineum, mesial side of the thigh, and practically the whole of the lower extremity. The remainder of the vessels of the femoral trunk (fig. 1, V. 1. fern.) continue caudally, following the femoral artery in its course in the leg.
Relation of the Peripheral Lymphatics to the Primary System.
I. Lymphatics arising ventral to the aorta.
A. Retroperitoneal sac.
1. Anterior portion.
(a) Cceliac trunk.
(I) Left branch.
(A) Mesial trunk.
(1) Adrenal (capsule) and kidney (ant. pole).
(2) Pancreas (body).
(4) Anterior anastomosis to thoracic duct.
(6) Trunk of lesser gastric curvature.
(a) ascending (left) periesophagus, cardia, diaphragm.
(6) descending (right) cardia, diaphragm, lesser curvature.
(B) Left trunk.
(1) Pancreas (tail).
(2) G astro-splenic trunk.
(a) Fundus of stomach.
(6) Splenic capsule.
(c) Vessels of greater gastric curvature ; (1) fundus; (2) pylorus.
(II) Right branch.
(A) Hepatic vessels.
(B) Right gastric vessels; (1) pylorus; (2) pancreas (body). (6) Lateral trunk.
(I) Portal vein. (II) Biliary ducts.
(c) Superior mesenteric trunk.
(I) Duodenal branch; (A) pancreas (head). (II) Mesenteric branch.
(d) Main anastomosis to cisterna chyli.
2. Posterior portion.
(a) Lateral branches. (I) Kidney. (II) Wolffian body.
(III) Genital branch.
(B) Wolffian body (caudal).
(C) Mullerian and Wolffian ducts.
(D) Caudal gonadal ligament.
(IV) Umbilical cord (medial side).
(V) Posterior anastomosis to caudal end of iliac sacs. (6) Medial branch.
(I) Descending colon.
II. Lymphatics arising dorso-lateral to the aorta.
A. Thoracic duct.
B. Cisterna chyh.
C. Iliac sacs.
4. Retrorenal branch.
5. Caudal portion.
(a) Anastomosis with retrorenal branch.
(b) Ilio-inguinal node.
(c) Lateral sacral branch.
(d) Posterior anastomosis with retroperitoneal sac.
(e) Posterior trunk.
(I) Proximal branches.
(A) Umbilical cord (lateral side).
(B) Wolffian body (posterior pole). (1) Mullerian and Wolffian ducts.
(II) Common iliac trunk.
(A) Hypogastric trunk.
(B) External iliac trunk; (1) sciatic vessels; (2) femoral vessels; (3) inguinal vessels.
The schema given on the preceding page shows graphically the relation of the peripheral lymph-vessels to the primary lymphatic system. In general the lym- phatics arising ventral to the aorta (the retroperitoneal sac) drain the whole or part of the lung, diaphragm, liver and biliary passages, stomach, small and large intes- tine, capsule of spleen, pancreas, kidney, gonad, Mullerian and Wolffian ducts, umbilical cord, and Wolffian body.
From the lymphatics arising dorso-lateral to the aorta (the iliac sacs) are supplied, either wholly or in part, the diaphragm, body-wall, adrenals, kidney, bladder, umbilical cord, Mullerian and Wolffian ducts, and the entirf posterior half of the body.
The structures which drain into the primary lymphatics arising both ventral and dorso-lateral to the aorta are the diaphragm, kidney, and Mullerian and Wolf- fian ducts.
RELATION OF THE LYMPH-GLANDS TO THE PRIMARY AND SECONDARY LYMPHATIC SYSTEMS
Sabin (1913) has shown that the primary lymph-nodes develop from the pri- mary lymph-sacs; that the pre-aortic or retroperitoneal glands develop from the retroperitoneal sac; and that from the iliac sacs there arises a chain of small nodes lateral to the aorta and a large group of glands on either side of the aorta opposite its bifurcation. Dorsal to the aorta are the prevertebral nodes extending from the lower end of the cisterna chyli to the aortic bifurcation.
Of the secondary lymphatic nodes developing along the lymphatic vessels, she states that the mesenteric glands are secondary for the retroperitoneal sac. In the pig the secondary glands from the iliac sacs are simple and two in number the ilio-inguinal gland (very characteristic for this animal) and the inguinal group of glands.
In this study, injections, as nearly complete as possible, were made of pig embryos 20 cm. or more in length to determine what glands receive the drainage from the abdominal and pelvic viscera. At this stage the glands are easily seen in the gross and, by injecting the organs with india-ink, their relations to the different glands can be readily demonstrated. Figure 5 is a composite drawing of an embryo pig 20 cm. long, viewed from the ventral side, to show the grouping and positions of the various lymph-glands relative to each other and to the different abdominal organs. Those glands formed from lymphatics arising ventral to the a.orta are indicated in solid color; those from lymphatics dorso-lateral to the aorta are stippled. The glands along the vessels posterior to the bifurcation of the aorta, however, which are in solid black, belong to the group arising from lymphatics dorso-lateral to the aorta and were not stippled because of the perspective.
In the abdomen are glands the pre-aortic extending from above the cceliac axis to the bifurcation of the aorta. Anteriorly these are grouped into the cceliac (fig. 5. Lymgl. ccel.) and main mesenteric glands (Lymgl. mes. sup.) and posteriorly into the lumbar pre-aortics (Lymgl. praeaorticse) . Lateral to the aorta are the juxta-aortic glands; on the right side some are prevenous, others retrovenous, in relation to the vena cava (fig. 5). Posterior to the aorta are the prevertebral glands. Glands are formed along the external iliac artery and smaller ones about the internal iliac or hypogastric artery.
LymaJ lien. Lymql cv. min
Lymql.mes.eup. Lymql juxla-intes
Lymgl. praeven. Vena Cava Lymfjl.praevert.
Lyrrigl. i I. COTI. Lyrrigl. ilioing.
Lymql prae-aorficoa Ovorium
Flo. 6. Composite diagrammatic drawing viewed from the ventral side of a pig embryo 20 cm. long. The glands arising from the retroperitoneal sac are in solid color, those arising from the iliac sacs are stippled. However, the glands along the^vessels posterior to the bifurcation of the aorta, which are in solid black, belong^to.the group arising dorsolateral to the aorta, but were not stippled because of thejper- epective. Drawing made by J. F. Didusch.
The retroperitoneal sac is transformed into the glands of the coeliac axis and, at the origin of the superior mesenteric artery, into the main mesenteric glands and also into the preaortics, the prevenous, and part of the juxta-aortic glands. The iliac sacs become the retrovenous, prevertebral, and the remainder of the juxtaaortic glands. The glands constituting the large group opposite the bifurcation of the aorta, as well as the proximal iliac glands, are formed from the caudal ends of the sacs.
DRAINAGE OF THE VISCERA
It has been shown that in the earlier stages the stomach has three main systems of drainage: (1) the trunk of the lesser gastric curvature, (2) the gastrolineal trunk, and (3) the right gastric branch. This system is likewise indicated by the lymph- glands, the three main channels of drainage being indicated by arrows in figure 5.
1. In a pig of 20 cm., when the injection is made about the periesophageal region, the vessels shown on the anterior side of the fundus and about the cardiac orifice drain around the neck and then posteriorly to several large nodes situated slightly posterior and to the left of the orifice on the pillar of the diaphragm (fig. 5, Lymgl. fundi.). Other lymphatic vessels, more from the middle portion of the stomach, drain to a gland on the right of the cardiac orifice (Lymgl. c. v. min.).
2. Lymph from the inferior part of the fundus drains along the posterior margin of the splenic ligament, following the lesser gastric vessels of the lienal artery, where it empties into several glands lying in the splenic ligament. From these nodes it drains posteriorly into several large glands near the left periesophageal glands (fig. 5, Lymgl. fundi). Part of the lymph from the greater curvature drains with that from the gastro-epiploic vessels to the middle region of the spleen, where it enters several glands. Connection is demonstrated between these glands and nodes situ- ated along the splenic vessel. Not only these glands, but also the periesophageals, follow the splenic artery to the cceliac axis (fig. 5, Lymgl. ccel.). From the superior and inferior medial regions of the stomach, vessels run toward the lesser curvature, along with the branches of the left gastric artery, to drain with a number of smaller nodes which are located to the left of the esophageal ring (fig. 5, Lymgl. c. v. min.) and drain, along with the right periesophageals, to the glands about the cceliac axis.
3. Lymphatics injected on the superior surface of the stomach near the pylorus drain in the direction of the lesser curvature, but run in the lesser omentum, turning with the vessels and emptying into very large glands situated along the hepatic artery (fig. 5, Lymgl. hep.). These hepatic glands also have as afferents the vessels of the greater curvature ; that is, the lymphatics of the greater curvature pass toward the pylorus accompanying the right gastro-epiploic artery (fig. 5, Lymgl. gastroepip.), following that vessel from its junction with the gastro-duodenal to the hepatic artery, where they drain into these large nodes. Thus, about the cceliac axis are a number of glands that in the earlier stages were in the form of trunks from the anterior end of the retroperitoneal sac, and they, too, show three main systems of drainage a left, a mesial, and a right.
In the lesser omentum are small lymph-glands draining part of the liver. The drainage from these nodes is seen to accompany the vessels from the pylorus which follow the right gastric artery to empty also into the large hepatic glands, and from these into the cceliac glands. When the gall-bladder was injected, some vessels were seen to follow the course of the common duct to the duodenum, then to accompany the portal vein to one of several large nodes situated about that vessel in the angle of the pancreas (fig. 5, Lymgl. d. choled.). Smaller glands were also seen along this vein peripheral to the larger ones. The efferents from these glands go to one or two pre-aortic nodes lying between the coeliac axis and the superior mesenteric nodes (fig. 5). Here, too, as in the earlier stages, there is a double drainage of the liver.
In these later stages the lymphatics of the spleen failed to inject. Those of the ligament, however, drain into glands at the hilum, from which the efferent flow is through glands which are disposed about the splenic artery.
The small intestine, large intestine, and descending colon drain into the large mesenteric glands, of which there are several groups. The largest and most im- portant of these are the juxta-intestinal glands (fig. 5, lymgl. juxta-intes.) which are the first to receive the lymph coming from the intestine. They are very large prominent, elongated glands, lying close together, their long axes parallel to that of the intestine. They form a distinct nodular rim or collar to the outer part of the mesentery. Efferents from the juxta-intestinal nodes pass through intermediate glands in the mesentery about the origin of the superior mesenteric artery (Heuer, 1909). These retromesenteric glands then receive afferents from the head of the pancreas, duodenum, and intestine. This system of secondary lymph-glands of the intestine, with the peripheral nodes very large and prominent, and the proximal ones smaller and very limited in number, is quite a contrast to the system of the stomach and neighboring organs, in which the glands increase in size and impor- tance the nearer they approach to their termination about the coeliac axis.
The lymphatics of the pancreas could not be injected directly, but there are indications that this organ has at least four collecting trunks: (1) The drainage from its tail is to the splenic group of glands; (2) the posterior part of the body sends some efferents to the periesophageal nodes; (3) the duodenal portion drains along with the lymph from the pyloric portion of the stomach to the large hepatic nodes; (4) the head of the pancreas sends efferents to the superior mesenteric glands. Bartels (1906) was able to inject the lymphatics of the pancreas in new- born animals, especially the dog, and in a later paper (1907) he described their drainage into the regional glands, which, in general, corresponds to the drainage indicated above.
It is evident from the earlier stages that the adrenals have a capsular drainage to the cceliac group of glands, while the lymph from the organ itself drains into a gland formed from the cephalic end of the iliac sac, i. e., a juxta-aortic gland which is seen lying anterior to the renal glands (fig. 5, Lymgl. g. suprar.).
Although not definitely determined, it would seem from the double type of earlier injections that the lymphatics from the kidney would drain into the pre- aortic and perhaps post-aortic, but mainly into the juxta-aortic glands. Several large nodes can be easily seen at the hilum lying behind the renal vessels, suggesting their origin from the iliac sacs, and a fairly large node anterior to the vessels suggests its origin from the retroperitoneal sac. The separation of the juxta-aortic glands by the vena cava, into a prevenous and a retrovenous group which were formed from lymph-sacs ventral and dorso-lateral to the aorta, is shown in the right side in figure 5, where the double drainage from the kidney to these two sets of glands at the hilum is indicated.
In young embryos, vessels from the region of the inferior mesenteric artery pass to the colon, and in later stages glands are seen about the inferior mesenteric artery, evidently draining the descending colon.
The drainage from the ovaries and testes is by vessels that accompany the correspondingly named arteries, first through one or two secondary nodes, then to the lumbar region, where these lymphatic trunks turn medially and run toward their terminal glands, which are situated ventral or ventro-lateral to the aorta and vena cava, extending from the bifurcation of the aorta to about the level of the posterior pole of the kidneys; that is, to pre-aortic, prevenous, and juxta-aortic glands in the lumbar region. To these same glands drains part of the lymph from the body of the uterus and Fallopian tubes in the female and from the epididymis in the male. These glands have been formed from the root of the genital branch as it comes off from the posterior end of the retroperitoneal sac (fig. 1, V. 1. gon.). When the horns of the uterus are injected, the flow is both toward the cervix and peripherally toward the tubes. The medial portion of the horn and part of the cervix drain to a very large gland at the bifurcation of the external and internal iliac arteries. Thus the lymph from the sexual glands has only one channel of flow, i. e., to the glands that were formed from the posterior portion of the ventral or retroperitoneal sac. The lymph from the excretory canals of the sex-glands, on the other hand, has a double course of flow; that from the structures originating proximal to the sex-glands goes to the glands formed from the ventral sac, while the portions of the excretory canals distal to the sex-glands drain to glands arising from the primary lymphatics dorso-lateral to the aorta.
Injections of the bladder showed lymphatics draining to the external iliac glands. Drainage from certain regions of the bladder passed through intermediate lateral vesicle glands peripheral to the iliac nodes. Occasionally a vessel could be injected to the glands at the bifurcation of the aorta.
The lymphatics from the posterior trunk of the iliac sac become transformed into a chain of lymph-glands which are disposed fairly regularly about the blood- vessels (fig. 5, Lymgl. il. com.). In general, they are similar to those described by Poirier and Cuneo (1904), except that there is a characteristic ilio-inguinal node in the pig which is not seen in man.
The inguinal glands drain the superficial lymphatics over the lower abdomen, external genitalia, ventral side of the tail, the leg, and the medial side of the thigh. The efferents of the inguinal glands are distal external iliac nodes.
An ilio-inguinal node (fig. 5, Lymgl. ilio-ing.), characteristic of the pig, lies in the course of the ilio-lumbar artery near the crest of the ilium. It drains the super- ficial lymphatics of the posterior body-wall, down over the hip and the root of the tail (Sabin, 1904).
In the posterior half of the body, the first stage in the formation of a connected, well-developed primary lymphatic system in the pig is the presence of primary lymph-sacs, lying ventral and dorsal to the aorta. The ventral sac is the large retroperitoneal sac, which extends from the region of the cceliac axis to the bifurca- tion of the aorta. Dorsal, or dorso-lateral, to the aorta is the remainder of the primary system the paired iliac sacs which extend from the region of the adrenals to the bifurcation of the aorta.
According to their origin from these primary sacs, lymphatic vessels t>f the organs and structures in the abdominal and pelvic regions fall into two great groups, dependent upon whether they arise from the primary lymphatics ventral to the aorta, or from the primary lymphatics dorso-lateral to the aorta. As a general statement, it may be said that the ventral sac supplies the abdominal viscera, while the dorso-lateral sacs supply the retroperitoneal structures the viscera, the body-wall, and the lower extremities although, on account of consider- able overlapping, this generalization must be regarded as only approximate.
Thus, from the retroperitoneal sac are given off lymphatics which drain the whole or part of the lung, diaphragm, liver and biliary passages, stomach, small and large intestine, capsule of spleen, pancreas, kidneys, Wolffian bodies, gonads, Miil- lerian and Wolffian ducts, and umbilical cord. The dorso-lateral lymphatics that is, the paired iliac sacs drain wholly or in part the diaphragm, body-wall, adrenals, kidneys, bladder, Miillerian and Wolffian ducts, umbilical cord, and the entire posterior half of the body. Only a few structures, notably the diaphragm, the kidneys, and the Miillerian and Wolffian ducts, which later become the excretory canals of the sex-glands, have lymphatics arising from both the ventral and the dorso-lateral sacs.
On following the development of the lymphatics in these posterior regions of the body, this early system of drainage is found to continue into the adult stage of lymphatic growth. The primary sacs change into lymph-glands which receive afferent vessels from the same organs and structures as did their parent sac. To a considerable extent the position of the primary lymph-glands, differentiated from the primary sacs, falls into two groups the glands ventral and ventro-lateral to the aorta, and those dorsal and dorso-lateral to the aorta. Here, too, in the adult stage of lymphatic growth, the general statement can be made that the organs and structures situated within the abdominal cavity have their lymphatic drainage into the group of glands whose position is ventral or ventro-lateral to the aorta. On the other hand, those structures and organs lying outside of the abdominal cavity, as well as the entire posterior half of the body, have their lymphatic drainage eventually into the group of glands situated dorsal or dorso-lateral to the aorta.
A. il. com.,
D. omph. mes.,
Lig. caud. gon.,
Lig. cran. gon.,
Lig. diaph. meson.,
Lig. genitoing. Lymgl. coel., Lymgl. c. v. min.,
Lymgl. d. choled.,
Lymgl. gl. suprar.,
Lymgl. il. com.,
Lymgl. juxta infest.,
Lymgl. juxta aortica
Lymgl. meg. sup.,
common iliac artery.
caudal gonadal ligament.
cranial gonadal ligament.
diaphragmatic ligament of the
mesonephros. genito-inguinal ligament, cceliac lymph-gland, lymph-gland of le&ser curvature of
lymph-gland of biliary duct, lymph-gland of fundus. gastro-epiploic lymph-gland, suprarenal lymph-gland, hepatic lymph-gland, common iliac lymph-gland, ilio-inguinal lymph-gland, juxta-intcstinal lymph-gland, juxta-aortie lymph-gland, splenic lymph-gland, superior mesenteric lymph-gland, pre-aortie lymph-glands, prevenal lymph-glands, prevertebral lymph-glands, retrovenal lymph-glands, mesonephros. ilio-inguinal node, oesophagus, orifice of ureter, oviduct, pylorus.
retrorenal branch, rectum, kidney.
S. il. pars caud.,
T. c. v. min.,
T. gast. dex., T. gastrolien., T. hypo., T. il. com., T. il. ext., T. mes. sup., T. post., Ur., V. 1. asc. duo.,
V. 1. cap. gl. suprar.,
V. 1. caput pan., V. 1. corp. pan., V. 1. coli des., V. 1. c. maj.,
V. 1. c. min.,
V. 1. diaph.,
V. 1. fern.,
V. 1. fundi,
V. 1. gl. suprar.,
V. 1. gon.,
V. 1. hep..
V. 1. h. mebon.,
V. 1. ing.,
V. 1. mes.,
V. I. pulrn.,
V. 1. pyl.,
V. 1. rect.,
V. 1. ren.,
V. 1. sacr. lat.,
Vena omph. mes.,
caudal part of iliac sac.
trunk to the lesser curvature of stomach.
right gastric trunk.
common iliac trunk.
external iliac trunk.
superior mesenteric trunk.
lymph-vessel of the ascending du- odenum.
lymph-vessel of the suprarenal capsule.
lymph-vessel of head of pancreas.
lymph-vessel of body of pancreas.
lymph- vessel of descending colon.
lymph-vessel to greater curvature of stomach.
lymph-vessel to lesser curvature of stomach.
lymph-vessel of diaphragm.
lymph-vessel of fundus.
lymph-vessel of suprarenal gland.
lymph-vessel at hilum of mesone- phros.
lymph-vessel of rectum.
lateral sacral lymph-vessel.
BAETJEH, WALTER A., 1908. On the origin of the mesen- teric sac and thoracic duct in the embryo pig. Amer. Jour. Anat., vol. 8, 303.
BARTEI.S, PAUL, 1906. Ueher die Lymphgefasse des Pankreas. II. Das feinere Verhalten der lymphatischen Verbindungen zwischeu Pan- kreas und Duodenum. Arch. f. Anat. u. Physiol., Anat. Abth.
, 1907, Ueber die Lymphgefasse deg Pankreas.
III. Die regionaren Drilsen des Pankreaa beim Menschen. Ibid., Anat. Abth.
CASH, J. R., 1917. On the development of lymphatics in the heart of the embryo pig. Anat. Rec., vol.
, 1921. On the development of the lymphatics in
the stomach of the embryo pig. Contribu- tions to Embryology, vol. 13, Carnegie InsL. Wash. Pub. No. 276.
CLARK, A. H., 1912. On the fate of the jugular lymph-sacs, and the development of the lymph-channels in the neck of the pig. Amer. Jour. Anat., vol.
CLARK, E. R. and E. L., 1920. On the origin and early development of the lymphatic system of the chick. Contributions to Embryology, vol. 9, Carnegie Inst. Wash. Pub. No. 272.
CUNNINGHAM, R. S., 1916. On the development of the lymphatics of the lung in the embryo pig. Contributions to Embryology, vol. 4, Carnegie Inst. Wash. Pub. No. 224.
HEUER, GEORQE J., 1909. The development of the lym- phatics in the small intrstine of the pig. Amer. Jour. Anat., vol. 9. 91.
HUNTINQTON, G. S., and C. F. W. McCLURE, 1910. The anatomy and development of the jugular lymph-sacs in the domestic cat. Amer. Jour. Anat., vol. 10, 177.
LEWIS, FREDERICK T., 1906. The development of the lymphatic system in rabbits. Amer. Jour. Anat., vol. 5, 95.
MALL, F. P., 1901. On the origin of the lymphatics of the liver., Johns Hopkins Hosp. Bull., vol. 12, 146.
POIRIER, P., and B. CUNEO, 1904. The lymphatics. Trana. by C. H. Leaf. Poirier and Charpy, Treatise of Human Anatomy.
SABIN, F. R., 1901. On the origin of the lymphatic system from the veins and the development of the lymph-hearts and thoracic duct in the pig. Amer. Jour. Anat., vol. 1, 367.
, 1904. On the development of the superficial
lymphatics in the skin of the pig. Ibid., vol. 3, 183.
, 1912. On thf origin of the abdominal lymphatics
in mammals from the vena cava and the renal veins. Anat. Rec., vol. 6, 355.
, 1913. The origin and development of the lym- phatic system. Johns Hopkins Hosp. Re- ports, monograph, new series, vol. 5.
, 1915. On the fate ol the posterior cardinal veins
and their relation to the development of the vena cava and azygos in the embryo pig. Contributions to Embryology, vol. 3, Car- negie Inst. Wash. Pub. No. 223.
, 1920. Studies on the origin of blood-vessels and
of red blood-corpuscles as seen in the living blastoderm of chicks during the second day of incubation. Contributions to Embryology, vol. 9, Carnegie Inst. Wash. Pub. No. 272.
STOCKARD, C. R., 1915. The origin of blood and vascular endothelium in embryos without a circulation of the blood, and in the normal embryo. Amer. Jour. Anat., vol. 18, 227.
STREETER, G. L., 1920. A human embryo (Mateer) of the presomite period. Contributions to Embryol- ogy, vol. 9, Carnegie Inst. Wash. Pub. No. 272.