Paper - The origin and early development of the posterior lymph heart in the chick (1915)

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West R. The origin and early development of the posterior lymph heart in the chick. (1915) Amer. J Anat. 17(4): 402-436.

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This historic 1915 paper by West describes development of the posterior lymph heart in the chick. Lymph hearts function as small pumps to pump lymph that has leaked out of the circulatory system back into the circulatory system. Found in lungfishes, all amphibians, reptiles and flightless birds.



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Crossley DA & Hillman SS. (2010). Posterior lymph heart function in two species of anurans: analysis based on both in vivo pressure-volume relationships by conductance manometry and ultrasound. J. Exp. Biol. , 213, 3710-6. PMID: 20952620 DOI.
PubMed Search: chicken thoracic duct development | thoracic duct development

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The Origin And Early Development Of The Posterior Lymph Heart In The Chick

Randolph West

Frotn the Laboratories of Comparative A natomy, Princeton and Columbia Universities

Fourteen Figures

Introduction

During the autumn of 1912 Professor McClure suggested to the writer the advisability of working out the early development of the posterior lymph heart in the chick, with especial reference to the source of its endotheUum. Throughout the following winter the problem was carried on under Professor McClure's supervision at Princeton University, while during the past year it has been continued under the direction of Professor Huntington at Columbia University.

Sala (1) in 1900 described the development of the posterior lymph heart of the bird, and gave a review of the literature to that date. In the caudal sections of an embryo of six days and eighteen hours incubation he finds that:

In the mesencliyme which stands in the lateral relation to the caudal myotomes and corresponds to the lateral branches of the first five coccygeal veins, a progressive excavation occurs of little spaces or fissures which soon enter into communication with the lateral venous branches themselves — one would say in fact that these fiSsures are onl}^ simple dilatations and ramifications of the veins themselves.

If the writer interprets him correctly, Sala states that the l3'mph hearts are formed b}^ an addition of spaces to the veins, and then a few lines later intimates that these spaces might be considered as ramifications of the veins themselves." He also states that the 'fissures' are at first few in number and are arranged in a linear series, parallel to the axis of the vertebral column, correspending to the point of penetration of each venous branch of the intermuscular septum, and that afterward they gradually increase in nmnber and come to lie near each other. He points out that at the end of the seventh day many of the little 'fissures' have fused to give rise to larger spaces, so that the spaces, separate at first, have finally established irregular communications between themselves, by breaking down their mesenchymal partitions. He goes on to show that by the end of the eighth day the ensemble of the cavities is transformed into a kind of a sac, still communicating with the first five coccygeal veins and later with the general lymphatic system, which develops independently by fusion of intercellular mesenchymal spaces at first appearing along the veins of the hypogastric plexus. The cavities at this stage often contain red blood cells and sometimes appear quite full of them, and by a condensation of mesenchymal cells the wall of the lymph hearts are formed. The rest of this paper, which does not especially concern us, shows that the lymph hearts increase in volume up to the sixteenth day, that the first and fifth coccygeal veins lose their connections with the hearts during this period, and that the connection of the lymph hearts with the independently developed general lymphatic system occurs toward the end of the tenth day. During the remainder of embryonic life the lymph hearts persist, but shortly after the chick is hatched they commence to degenerate. Traces of the degenerating lymph hearts were found in a chicken thirty-five days after hatching.

Alierzejewski, in 1909 (2), published an article on the origin of the lymphatic vessels in birds, which was presented by M. H. Hoyer before the Academy of Sciences of Cracow. Concerning the origin of the posterior lymph hearts he agrees with Sala, except that he holds that the first anlagen appear in the middle of the sixth day of incubation, and not, as Sala states, in the first hours of the seventh day.

Stromsten (3) has published two papers in 1910 and 1911 on the development of the posterior lymph heart in turtles. He finds that their development is initiated in the logger-head turtle by the vacuolization of the post-iliac mesenchymal tissue during the latter part of the second week of development, and that the spongy tissue thus formed is invaded by capillaries from the dorso-lateral branches of the caudal portion of the postcardinal veins. The capillaries do not communicate primarily with the mesenchymal spaces. Near the close of the third week, parallel veno-lymphatic channels are formed in this spongy area by the confluence of mesenchymal spaces with one another and with the invading capillaries. These veno-lymphatics anastomose freely with each other and communicate by two or three openings with the veins running along their mesial borders. Finally a condensation of mesenchyme and an invasion of muscle cells form the wall, while a confluence of the venolymphatic sinuses gives rise to the single sac-like cavity of the adult form of the lymph heart.

The subject rested at this point until 1912 when E. L. Clark (4) cited observations, based on injections, to show that in the chick of five days and twenty hours, in the region later occupied by the posterior lymph heart, there exists a lymphatic plexus connected with the coccygeal veins, but not with the haemal capillaries which bear a superficial relation to the lymphatic vessels. She also shows that the lymphatic plexus is of a different pattern than the blood capillary plexus and is filled with stagnant blood, which she considers as backed up from the coccygeal veins. This state of affairs undoubtedly exists in the chick of five days and twenty hours but the observation, aside from its morphological value, throws no light on the origin and mode of growth of the lymphatic plexus.

E. R. and E. L. Clark (5) in a paper in the same number of The Anatomical Record attempt to prove, by observing the first appearance and early growth of this blood filled lymphatic plexus in the living chick embryo of about five days, that it is formed by a purely centrifugal outgrowth from the coccygeal veins. To quote from their article:

The first lymphatics in the tail region of the chick arise as direct lateral buds from several of the main dorsal intersegmental coccygeal veins, and not by the transformation of a previously functioning blood vessel plexus. From now on the lymphatic endothelium is specific and spreads by a steady centrifugal extension * * * * The buds send out processes forming clusters. From the clusters, in turn, processes are sent out which anastomose with one another, forming a plexus. Simultaneously^ processes grow toward the surface from the clusters, and give rise to the superficial plexus of peripheral lymphatics of the posterior part of the body. There is no essential difference between the manner of growth of the peripheral lymphatics and that of the plexus which is to form the lymph heart (p. 258).

In June 1913 Miller ((3) in a preliminary note on the development of the thoracic duct of the chick states that certain aggregations of mesenchymal cells mentioned by Sala (1) "comprise developing blood cells which are differentiated in situ out of the indifferent mesenchymal syncytium, that these blood cells then gain access to the lymph channels making up the developing thoracic duct, and that finally the haemal cellular elements in question, reach the blood stream via the thoracic duct and the jugular lymph sac." He clearly recognizes that lymphatic channels may serve to transmit blood cells arising in situ in the mesenchyme to the haemal channels and distinguishes this function of the lymphatics by the term 'haemorphic' He further states that "the lymphatics arise as isolated lacunae directly from mesenchymal intercellular spaces and are not in any sense derived from the veins, and subsequently coalesce to form the continuous channel of the thoracic duct." The possibility of venous origin of these lymphatics or of the backing up of their blood content from the veins is excluded by the total absence of the azygos system in the Sauropsida. In his completed paper of September 1913 Miller (6) gives his results in greater detail. He states that the lacunae in question are bounded at first by indifferent mesenchymal cells which become flattened to form cells which are morphologically equivalent to endothelial cells.

Hoyer in June 1913 presented Fedorowicz's "Untersuchung iiber die Entwickelung der Lymphgefiisse bei Anurenlarven" (7) before the Academy of Sciences of Cracow. Fedorowicz, working on Bufo vulgaris, Bufo viridis, Rana esculenta, and Rana temjioraria found cell strands developing from the surface of the lymph heart. In these strands intercellular spaces and finally lumina, which could not be injected from the lymph heart, appeared. The lumen of each strand he found to be lined with endothelial cells. By the continuation of the space formation lymphatic vessels developed which connected secondarily with the similarly acquired lumina of other cell strands which had appeared within the heart. It was not until this connection was established that it was possible to inject the lymphatic vessels from the heart.

Allen (8) in a recent important publication on Polistotrema (Bdellostoma) describes the caudal lymph heart as arising from isolated mesenchymal spaces in the region of the anterior end of the two branches of the caudal vein, and the ultimate fusion of these spaces by the breaking down of their partitions. Incident to this process certain cells in the interior of the system of spaces become spherical and are transformed into red blood corpuscles. Secondarily the cavity of the lymph heart establishes connections with the caudal vein by the same process, that is a breaking down of mesenchymal partitions while peripherally the cavity is enlarged by the new formation of isolated mesenchymal spaces and their ultimate annexation. C'oincidentally the mesenchymal cells bordering the cavity of the lymph heart flatten to form its endothelium. Allen in conclusion says that his

  • * studies thus far indicate that the most primitive form of

lymphatic system are veins that function for both lymphatics and veins. Hence it would be expected that ontogeny would repeat the phylogeny of the lymphatics, and instead of having their origin directly from the veins, they would begin directly as the veins did, by the vacuolization of the original mesenchyme.

T'hese vessels Allen has designated 'veno-lymphatics.' The recognition of haemopoesis in the vicinity of developing lymphatics and from their endothelium is of major morphological importance and the substantial agreement between the results of Allen and of Miller should go far to clear up some of the difliculties that have beset the study of the ontogeny of the lymphatic system. The term veno-lymphatic was used by Huntington and McClure (9) in their studies of the mammalian jugular lymph sac to designate constituents of the sac which were found at first to contain blood and later to be devoid of blood content. The term veno-lymphatic was simply meant to cover these two conditions of the vessels; for at the time of their studies the criterion of content seemed most available to discriminate between lymphatic and haemal channels. The work of Miller and of Allen demonstrating the i7i situ formation of blood cells and their carriage by lymphatics affords a complete and satisfactory explanation of these earlier observations, and Miller's term haemophoric lymphatic satisfactorily describes the actual conditions, and it is to be hoped in interest of clarity will replace veno-lymphatic. This question was fully considered by Huntington (10) at the Thirtieth Session of the American Association of Anatomists.

The present investigation is concerned with the earliest appearance of the posterior lymph hearts in the chick. They are two in number and bilaterally symmetrical. Each one arises in the mesenchyme lateral to the caudal rriuscle plate and posterior to the hind limb bud. Before the lymph heart assumes the form of a single sac-like cavity there exists in this same area a plexus of lymphatic vessels which later coalesce to form the single cavity of the lymph heart. Both the completed lymphatic plexus and later the lymph heart are in connection with several of the most anterior coccygeal veins by means of their lateral branches which pierce the caudal muscle plate, drain the lymphatics, and then pass outward in the younger embryos to drain a haemal capillary plexus, which bears a superficial relation to the lymphatic plexus.

It is the purpose of this paper to show that the plexus of lymphatic vessels, which later enters into the formation of the posterior lymph heart arises by the confluence of independent mesenchymal spaces which connect secondarily with the veins; that these spaces are bounded at flrst by mesenchymal cells which become flattened to form an endothelium, and that both in the endothelial lymphatic walls and in the adjacent mesenchyme an active haemopoesis is taking place.


Material

Forty-one of the forty-five embryos used in this work were injected with India ink through the large vitelhne blood vessels, the injection usually being pushed to the point of extravasation for the haemal capillaries. Of the four embryos not injected


Template:West1915 table1

TABLE 1


List of sectioned


embryos



Length in mm. after fixation


Age in days


Hours


Series


6.75


4


12


371


7


4


16


32A


8


4


16


31A


8.5


4


18


5A


8.5


4


18


33A


8.5


4


20


21A


9


4


18


29A


9


4


20


27A


9


4


20


23A


9


4


21


22A


9


4


21


4A


9


5


1


7A


9.5


4


18


30A


9.5


4


18


28A


9.5


4


20


24A


9.5


4


20


8A


10


?


?


13A


10


4


21


9A


10.5


4


20


26A


10.5


4


20


25A


11


4


21


20A


11


5



12A


11


5


1


6A


11


5


13


2A


11.5


5


7


ISA


11.5


5


7


19A


11.5


5


3


14A


11.5


5


1


lOA


12


5


6


34A


12.5


5


10


326


13.5


6


1


lA


13.5


?



3A


14


5


20


17A


14.5


?



llA


15


5


20


15A


15


5


20


16A


through the vitelline vessels three were injected directly into the posterior lymph heart plexus and one (12 mm.) was not injected at all. All material was fixed in Zenker's fluid. Thirtysix of the embryos were cut into 10 yu and 7 m serial sections and stained on the slide with eosin and methyl blue by Mann's method. One or two series were stained with Delafield's hemotoxylin and orange G, but this method gave a very poor differentiation of the blood cells. The nine embryos not sectioned were cleared by the Spateholz method and examined in tola imder the binocular microscope (table 1).

Observations

A. Formation Of Blood Cells From The Mesenchyme And Their Entrance Into The Circulation Via The Developing Haemal Capillaries, Prior To The Formation Of Lymphatics

As the appearance of numerous })lood cells in the mesenchyme and the extension of the haemal capillaries, previously referred to, is the first change which occurs in the mesenchyme lateral to the caudal muscle plate in the caudal region of the embryo, these processes will be considered first. When the lymphatic anlagen first appear, in the 10.5 mm. embryo, the haemal capillary plexus has reached a very high degree of complexity and from this time onward merely holds its own or develops comparatively slowly.

The youngest embryo examined was one of 6.75 mm. In this specimen the mesenchyme lateral to the muscle plate was uniformly loose, and very nearly indifferent. A few rather rounded eosinophile cells were observed in each section. Some of these cells contained one or two large eosinophile granules. Occasional venous branches pierced the muscle plate to drain the mesenchyme lateral to it.

The same area in the 7 mm. embryo presents several changes. The mesenchyme is much more compact, being equal in density to the mesenchyme which lies medial to the muscle plate. Groups of differentiating blood cells are much more abundant.

These cells are becoming rounded, with a diameter of 7 to 8 ix. Their cytoplasm is neutrophile or eosinophile and contains several strongly eosinophile granules. The nucleus is slightly more basophile than the cytoplasm. Eosinophile granules were also observed in the cytoplasm of some of the mesenchyme cells. There is usually a free space of 2 to 3 m about each differentiating cell, which is not encroached upon by the surrounding mesenchyme. Lateral branches of the coccygeal veins pierce the caudal muscle plate at regular intervals but the capillaries which they drain are few in number.

The 8.5 mm. embryo presents a very similar state of affairs, except that the capillaries emptying into the lateral branches of the coccygeal veins are somewhat more numerous, and the differentiating blood cells also occur in greater numbers. As may be seen from figure 1, 5, the haemal capillaries are injected to the point of extravasation, but the dift'erentiating eosinophile cells (7) are absolutely independent of them, nor are there any eosinophile cells medial to the caudal muscle plate.

From this stp.ge on until the embryo reaches the length of 10.5 or 11 mm. (fig. 2), the capillary plexus steadily increases in richness and complexity, while the blood cells differentiating from the mesenchyme become scarcer. The capillary plexus has invaded the area formerly occupied by differentiating blood cells, and blood cells in the mesenchyme have decreased until only a small fraction of those present in the 8.5 mm. embryo remain .

These blood cells have, then, either degenerated and disappeared, or have been drained off by the capillary plexus. The present investigation has not been of such a character as to warrant tracing the complete history of the blood cells which differentiate from the mesenchyme but representatives of both the red and white blood cell lines have been identified in the tissue spaces.

That these cells are drained off by the extending capillaries is indicated by the fact that within five or six hours we find first a practically indifferent mesenchyme, a little later a ver}^ active haemopoesis taking place in it and finally a general vas cularization of the tissue accompanied by a marked decrease in the number of blood cells in the tissue spaces. It seems highly improbable that decided haemopoesis should take place only to let the cells formed disintegrate three or four hours later without having entered a vessel, and moreover none of the blood cells observed in the tissues appeared to be disintegrating. McWhorter and Whipple (11) in their study of the chick blastoderm in vitro have observed a to-and-fro movement of the blood cells in the tissue spaces synchronous with the heart beat, and have also observed the entrance of these cells into the general circulation following their rhythmical movement. This phenomenon might be regarded as a plasmatic pulse, which would eventually force any blood cells lying free in the tissue spaces into the general circulation. In addition those cells having the power of amoeboid movement could enter the vessels by diapedesis through the capillary walls.

B. Development Of The Lymphatic Plexus And Accompanying Haemopoesis

The changes about to be described take place only in the mesenchyme lateral to the caudal muscle plates in the posterior region of the embryo, the mesenchjane lying medial to the muscle plates maintaining its compact indifferent character. For the sake of clearness we shall first consider the Histogenesis and then the Morphogenesis of the developing plexus of lymphatic vessels.


Fig. 1 Chick 8.5 mm., Series 21, Slide 1, Row 3, Section 2. X 200. Photomicrograph of transverse section of caudal end of the embryo.

1, Notochord 5, Haemal capillaries

2, Neural tube 6, Caudal muscle plate

3, Coccygeal vein 7, Differentiating blood cells

4, Coccygeal artery


1. Histogenesis

In the embryo of 10.5 mm. (about 4 days and 22 hours) we observe two new phenomena; the formation of spaces bounded by mesenchymal cells which eventually become flattened to form an endothelium, and the appearance of certain strands of flattened cells in the mesenchyme. Haemopoesis continues to take place in the mesenchyme and also from endothelial cells of the lymphatic walls as soon as these are formed.

Throughout the younger stages until the embryo has reached the length of 10.5 mm. the mesenchyme lateral to the caudal muscle plate is of a uniform degree of compactness equal to that of the mesenchyme medial to the muscle plates. The 10.5 mm. embryo, however, shows a slight, but distinct loosening of the mesenchyme just lateral to the muscle plate, between the points of penetration of the lateral branches of coccygeal veins and at certain points the loosening of the tissue is more marked, giving rise to small mesenchymal spaces. The spaces still bounded by mesenchyme are more numerous in the 11 mm. embryo (fig. 2, 8) and some differentiating blood cells have become included in them (fig. 5, 7). Certain of the spaces nearest the veins have acquired a venous connection at this stage and in the injected embryos appear as small knob like processes (fig. 5, 10) of a larger caliber than the veins with which they connect, filled with blood cells, and lined by endothelium. These knobs correspond in shape to the mesenchymal spaces mentioned. It is to be expected that when a space connects with a vein and is subjected to the pressure and friction of the general circulation, that the cells bounding it will tend to become flattened. And the fact that in later stages, when the still isolated spaces become larger and are under a greater plasmatic pressure


Fig. 2 Chick 11 mm.. Series 20, Slide 1, Row 4, Section 3. X 200. Photomicrograph of transverse section of the caudal end of the embryo.

1, Notochord 5, Haemal capillaries

2, Neural tube 6, Caudal muscle plate S, Coccygeal vein 8, Mesenchymal space

4, Coccygeal artery 9, Lateral branch of coccygeal vein



the bounding cells do flatten, renders it highly probable that a similar process takes place in the case of the smaller spaces which fii'st acquire a venous connection.

As was pointed out by E. R. Clark (12) at the Christmas meeting of the Anatomical Society in 1913, there are present in the mesenchyme lateral to the caudal muscle plate in the posterior region of the embryo certain strands of flattened cells which Clark holds to be outgrowths from the venous endothelium and to be always capable of being traced back to the veins. These cells, he says, contain nuclei which may be distinguished from the mesenchyme nuclei by their morphological and staining characters.

That strands of flattened cells, sometimes with continuous lumina, sometimes with an interrupted lumen or with no lumen at all occur in the chick as early as 9.5 mm. and more abundantly in the later stages, is true. But that they can be clearly distinguished from mesenchyme cells, and that they can always be traced back to a venous endothehum, are at least open questions.

E. R. Clark (12) describes the endothelial nucleus as being rather pale and elongated with one or two definite reddish discoid nucleoli, while the mesenchymal nucleus he holds to be darker, and more chromatic with one or two irregular bluish nucleoli, not sharply differentiated from the surrounding chromatin material. A careful examination, however, reveals a series of graduated stages between these two forms of nuclei. A slight change in the focus of the microscope will make a bluish nucleolus appear reddish, and vice versa, while a careful study of the tissue reveals great variance in the amount of chromatin


Fig. 3 Chick 15 mm., Series 16, Slide 2, Row 4, Section 8. X 300. Photomicrograph of transverse section of the caudal end of the embryo.

), Notochord 7, Differentiating blood cells

^. Neural tube 8, Mesenchymal space

3, Coccygeal vein 9, Lateral branch of coccygeal vein

i, Coccygeal artery 10, Lymphatic connected with vein

0, Haemal capillaries 11, Aorta

6, Caudal muscle plate


in the various nuclei. That the typical nucleus of the fully differentiated endothelial cell may be distinguished from that of the indifferent mesenchyme cell we do not deny, but that intermediate stages between the two exist, in the case in question we likewise hold to be true. And unless it be cut parallel to its long axis, it is practically impossible to distinguish even the fully differentiated endothelial nucleus from the mesenchymal nucleus.

As for the statement that these flattened rows of cells are always connected with a preexisting endothelium it must be remembered that practically every cell in the embryo is, at this stage, in syncytial relation with every other cell, the blood cells excepted. So in a certain sense a -protoplasmic connection between flattened cells and preexisting endothelium may be demonstrated by passing over the protoplasm of indifferent mesenchyme cells. To assume that because all endothelium in the embryo is in syncytial relationship it is therefore derived from some preexisting endothelium, appears unwarranted. Can it not be said with equal truth that since the embryonic vascular endothelium is in syncytial relationship with the mesenchyme it is therefore derived from the mesenchyme? This being the case, we know that there are in the mesenchyme certain flattened cells which are not connected with any preexisting endothelium otherwise than by means of the protoplasm of the mesenchymal syncytium. The isolation of these flattened cells from any other endothelium and the fact that all possible gradations


Fig. 4 Chick 8.5 nun., iSeries 21, felide 1, How 3, Section 2. X oUU. 1 liotomicrograph of transverse section of the caudal end of the embryo.

Fig. 5 Chick 11 mm., Series 20, Slide 1, Row 4, Section 4. X 600. Photomicrograph of transverse section ot the caudal end of the embryo.

Figure 4. Figure 5.

S, Coccygeal vein S, Coccygeal vein

5, Haemal capillaries 5, Haemal capillaries

6, Caudal muscle plate 6, Caudal muscle plate

7, Differentiating blood cells 7, Differentiating blood cells

S, Mesenchymal spaces U). Lynii)hatic connected with \ein


exist between them and the typical mesenchymal cells shows clearly that an in situ differentiation of endothelial cells takes place (fig. 6, 13, and fig. 7, 19). The cells so formed may then bound isolated cysts filled with plasma (fig. 6, 12) which sometimes enclose a differentiating blood cell. These plasmatocysts then proceed to grow together connecting up with one another and with the veins, and it is probable that they form in some instances a connecting link between the veins and the large lacunae in the mesenchyme. The early appearance of the blood-filled lymphatic plexus connected with the veins in the living chick, which E. R. and E. L. Clark (5) describe as follows, lends weight to such an interpretation of the facts :

The first evidence of lymphatics in the tail region of the living chick is the appearance of separate knobs filled with stagnant blood just lateral to the coccygeal veins. Soon after these knobs appear similar ones develop about them which have fne connections with them.

  • * Their injection shows discreet tiny clusters, somewhat like bunches of grapes (p. 254).

Figure 6, a section of the caudal region of an 11 mm. embryo, shows an isolated plasmatocyst {12). This section and the adjacent sections were studied with the greatest care under the oil immersion lense, and the two elongated cells (IS) with pale nuclei and distinct nucleoli bounding the cyst were not in connection with any other endothelium.

Figure 7, a section of the caudal region of a 15 mm. embryo, shows a structure which some might describe as a venous sprout. The injection mass has entered the lumen for a short distance in large amounts. Then the lumen becomes somewhat constricted, and beyond that point only occasional ink granules can be found. Finally the lumen terminates and a long flat cell (IS) follows in which two distinct nucleoli are seen, beyond which is a space (15) bounded by a delicate strand of cytoplasm on either side. This space contains a differentiating red blood cell (7). The adjacent sections have also been examined with great care, and the one directly preceding shows one rather elongated flattened cell with a pale nucleus forming the floor and probably the end of the plasmatocyst containing the blood cell just described. Several of the mesenchymal cells near by, in the direction in which this 'sprout' would extend, show a tendency to become elongated {19), but they are separated from the endothelial cell by indifferent mesenchymal cells, and their nuclei are quite chromatic. They probably represent cells which are about to flatten and to limit a plasmatocyst.

Since disconnected plasmatocysts have been found; since all gradations between an indifferent mesenchymal cell and a typical endothelial cell have been observed; and since, in the section just described, we find most distally an uninjected plasmatocyst, containing a differentiating blood cell, then a single endothelial cell enclosing no lumen, and finall}^ a lumen connected with the veins into which the injection mass has entered, it does not seem justifiable to call this structure a venous sprout. It should rather be considered as a plasmatocyst which has differentiated in situ, and connected secondarily with the vein. Whether the endothelial cells between the plasmatocyst and the vein arise by an in situ differentiation, or by a mutual growth of the plasmatocyst and the vein toward each other, it is impossible in this particular case to determine definitely by the study of sections or injections. The latter interpretation would in no way invalidate the fundamental conception that endothelium arises in situ from mesenchyme. It merely implies that endothelial cells once formed are capable of proliferation, as cells in general are. It should be noted that discontinuity of the lumen of the 'sprout' present in figure 7 shows clearly the utter inadequacy of the injection method for demonstrating all of the endothelium in the embryo.

As regards the further development of the blind spaces in the mesenchyme, we have seen that in the 10.5 and 11 mm. embryos there exist a number of spaces in the mesenchyme just lateral to the caudal muscle plate, and that these spaces are bounded by mesenchymal cells. Some of these spaces are connected at this stage with the lateral branches of the coccygeal veins, and certain blood cells, differentiating from the mesenchyme, have become included in some of the disconnected spaces. In the 12.5 mm. and 13.5 mm. embryos more and more spaces continue to connect with the veins, either directly or by means of the delicate hollowed 'cell strands' already described, and as the spaces acquire venous connection, they may become filled with blood backed up from the general circulation especially in injected embryos. The spaces which have not as yet attained a venous connection, increase in size, several smaller spaces coalescing by a breaking down of their cell boundaries to form a single larger space (fig. 9, 8; fig. 8, 8; fig. 3, 8). As the plasmatic pressure becomes greater, the indifferent mesenchyme cells which bounded these spaces become flattened to form cells which are identical in appearance with endothelial cells (fig. 9, 8). The first spaces about which endothelial cells were detected were in a 13.5 mm. embryo, although the cells bounding the spaces were somewhat flattened in the 11.5 mm. and 12.5 mm. embryos. The fact that the cells about a single isolated space may be in part endothelial and in part mesenchymal, with many intermediate stages between the two, indicates that an in situ differentiation of endothelium from mesenchyme is taking place.

The haemopoesis, which was described as taking place before the lymphatic anlagen appear, continues, but much less rapidly than formerly. We have seen that the mesenchyme lateral to the caudal muscle plate was first practically indifferent and non-vascular. Then came a wave of haemopoesis, followed


Fig. 6 Chick 11 mm., Series 20, Slide 1, Row 3, Section 7. X 500. Photomicrograph ot transverse section of caudal end of the embryo.

Fig. 7 Chick 15 mm., Series 16, Slide 2, Row 4, Section 6. X 500. Photomicrograph of transverse section of caudal end of the embryo.

Figure 6 7, Differentiating blood cell

6, Caudal muscle plate ^> Mesenchymal space

9, Lateral branch of coccygeal vein , ^' Lateral branch of coccygeal vein

12, Isolated plasmatocyst ^^> Elongated cell with pale nucleus

13, Elongated cell with pale nucelus ^^^ distinct nucleoli

and distinct nucleoli ^^' Lumen continuous with vein

15, Lumen not continuous with vein ^^Sure 7 j^g^ Isolated flattened cell, with pale

3, Coccygeal vein nucleus and distinct nucleoli

6, Caudal muscle plate


quickly by a vascularization of the tissue and a decrease in the number of blood cells in the tissue spaces. This takes the embryo up to the 10.5 mm. stage, when the lymphatic anlagen first appear. From this time onward certain mesenchyme cells still seem to become rounded, break away from the surrounding syncytium, and acquire eosinophile granules. In other cells the cytoplasm becomes eosinophile more evenly, forming erythrocytes. These cells, which lie in the tissue spaces, for the most part become included in the lymphatic anlagen, and as these anlagen acquire a venous connection, reach the general circulation.

For the first time in the 12.5 mm. embryo groups of rounded strongly basophile cells, may be observed to be differentiating from the endothelium near the junction of the lymphatics and veins. Small clumps of rounded cells, more strongly basophile than the mesenchyme or endothelial cells, are seen forming and apparently splitting off from the endothelium of the lymphatics (fig. 10, 16). In some of the older embryos the cytoplasm of these cells accjuires an eosinophile tinge. These cells are identical with the erythroblasts described by Dantschakoff (13). Finally, in the 13.5, 14.5 and 15 mm. embryos large aggregations of slightly basophile cells with conspicuous eosinophile granules (fig. 11, 17) are seen differentiating and splitting off from the lymphatic endothelium.

One hnal point must be noted, although it does not concern the endothelium of the lymphatic plexus. In the 14.5 mm. embryo strands of three or four myoblasts appear in the now

Fig. 8 Chick 14 mm., Series 17, Slide 2, Row 1, Section 6. X 300. Photomicrograph of transyerse section of caudal end of the embryo.

Fig. 9 Chick 15 mm., Series 16, Slide 2, Row 4, Section 6. X 600. Photomicrograph of transverse section of caudal end of the embryo.

Figure 8 Figure 9

3, Coccygeal vein 3, Coccygeal vein

5, Haemal capillaries 6, Caudal muscle plate

6, Caudal muscle plate 8, Isolated space, bounding cells bc8, Mesenchymal space coming flattened

10, Lymphatic connected with veins 9, Lateral branch of coccygeal vein

10, Lymphatic connected with vein


vacuolated mesenchyme just lateral to the caudal muscle plate and parallel to the axis of the notochord, and occasional very small longitudinal spaces may be seen in the most lateral portion of the caudal muscle plate. In one or two sections, one end of the strand of myoblasts was seen to be in connection with the muscle plate. Whether these cells were splitting off from the muscle plate by delamination, or whether they were forming from the mesenchyme and being added to it by accretion, it was not possible to determine in the material available.

2. Morphogenesis

Up to this point we have considered the histogenetic changes which take place in the developing lymphatic plexus, and we shall now consider the morphogenesis of the plexus. For this purpose four wax reconstructions have been made by the method of Born, three of which are here reproduced.

Chick of 11 vim. Reconstructions of vessels and isolated spaces of the caudal region. X 150. Figure 12: Arteries black, veins and capillaries white, isolated spaces yellow. The postcardinal vein and the aorta run a few sections above the upper level of this reconstruction, but the coccygeal branches of the aorta (fig. 12, 4) and a little more externally the coccygeal veins {3) which drain into the postcardinals, are seen running downward at right angles and dorsal to the axis of the vertebral column. All of these structures are medial to the caudal muscle plate, which has been omitted from this reconstruction for the sake of simplicity. This muscle plate extends in a plane, parallel to the ectoderm, just lateral to the coccygeal veins. Two or three lateral branches of each coccygeal vein (fig. 12, 9) pierce the muscle plate and proceeding directly outward terminate in a plexus of haemal capillaries which lie directly beneath the ectoderm.


Fig. 10 Chick 12 mm., Series 46, Slide 1, Row 4, Section 4. X 500. Photomicrograph ot transverse section of caudal end of the embryo. Uninjected.

Fig. 11 Chick 15 mm., Series 16, Slide 2, Row 4, Section 7. X 600. Photomicrograph of transverse section of caudal end of the embryo.

Figure 10 Figure 11

3, Coccygeal vein 5, Haemal capillaries

6, Caudal muscle plate 17, Blood cells differentiating from

16, Blood cells differentiating from lymphatic walls endothelium


The lymphatic plexus, which later forms the lymph heart, develops in the mesenchyme between the caudal muscle plate and this superficial plexus of haemal capillaries. A nmnber of isolated spaces, bounded by mesenchyme cells which are still practically unflattened, are seen (fig. 12, S; fig. 5, 8) to occupy the position just alluded to. They have been studied very carefully with oil iniinersion lenses and are absolutely independent of any vascular connection, either v/ith the lateral branches of the coccygeal veins or the haemal capillaries; they occur only caudal to the level of the hind limb bud and only lateral to the muscle plate.

Chick of 14 mm. Reconstruction of the blood vessels of the caudal region, and the lymphatic plexus in so far as it forms a continuous channel connected with the veins. X 150. Figure 13: Arteries black, veins and capillaries white, lyniphatics connected with veins, green. The isolated spaces have been omitted from this reconstruction in order that the lymphatic plexus connected with the veins might be more clearly shown. The reconstruction has been drawn from the side and somewhat from above and the aorta and postcardinals have been shown in the drawing as folded upward and outward. We have in this reconstruction practically the same arrangement of a.rteries, veins and haemal capillaries as was described for the 11 mm. embryo. The two postcardinal veins (fig. 13, 18) are seen above and somewhat lateral to the aorta; they anastomose above that vessel, and receive the coccygeal veins both cranial and caudal to their anastomosis. The coccygeal veins (fig. 13, 3) as before, pass downward, at right angles to the axis of the vertebral colu nn, close to the caudal muscle plate, and give off lateral branches (fig. 13, 9 a, b) which pierce the muscle plate. It will be seen that a plexus of lymi)hatic vessels connected with the coccygeal veins has been established between the haemal capillaries and the muscle plate, which is chai-acterized by the irregular size of its vessels, prominent knob-like enlargements occurring whereever a large independent space previously existed. This plexus, as has been noted, usually fills with stagnant blood, backed up from the venous circulation. There is no connection between the lyraiphatic plexus and the haemal circulation except at the point where the lateral branches of the coccygeal veins have just pierced the muscle plate.

We now see that the lateral branches of the five or six most cranial coccygeal veins pierce the muscle plate, drain the lymphatic plexus and then pass outward to drain the haemal capillary plexus (fig. 13, 9a). Soon that portion of the lateral branches of the coccygeal veins distal to the I3 mphatic taps degenerates, thus severing the connection of these veins with the haemal capillaries, so that those lateral coccygeal branches which drain the lymphatic plexus, cease to function otherwise than for the lymphatic drainage (fig. 13, -96). An examination of several injected embryos cleared by the method of Spateholz showed this point clearly; the haemal capillary plexus being drained in the 15 mm. embryo by the most dorsal portions of the coccygeal veins with only two of the lateral coccygeal branches assisting them, although in the embryo of 11.5 mm. five or six lateral coccygeal branches drained the plexus of haemal capillaries. One 17.5 mm. embryo which was examined in cross sections, showed no connection between the lateral branches of the five or six coccygeal veins which drain the lymphatic plexus and the haemal capillaries.

Chick of 15 mm. Reconstruction of the caudal vessels. X 150. Antero-lateral view. Figure 14- Arteries black, veins and capillaries white, lymphatics connected ivith the veijis green, isolated spaces yellow. In this reconstruction the coccygeal veins (3) are seen extending downward from the postcardinals {18) and the coccygeal arteries (4) from the aorta {11). The coccygeal veins give off lateral branches {9) which pierce the caudal muscle plate — which has been omitted from this reconstruction — and then proceed laterally to drain the lymphatic plexus (green) and at the points where the lymphatics are not as yet formed to any extent, the haemal capillary plexus (white). The lymphatic plexus may be clearly seen to occupy the area which in the reconstruction of the 11 mm. chick was filled only by isolated mesenchymal spaces. A great number of these isolated spaces (yellow, 8) still exist, not connected as yet with the lymphatic plexus. They occur in greater numbers medial to the lymphatic plexus which is connected with the veins (green, 10) that is between it and the caudal muscle plate, than they do lateral to the lymphatic plexus, although quite a number, as may be seen from the figure, occup}^ the latter position. It is especially interesting to note that the isolated spaces lie on all sides of the lymphatic plexus, seeming to precede it and form in an area which an hour or two later is occupied by the continuous plexus of lymphatics, connected with the coccygeal veins. Such outlying isolated spaces are clearly shown at the cranial end of this reconstruction.


Fig. 12 Reconstruction of caudal vessels of a chick of 11 mm., Series 20. X 150. Antro-lateral view; arteries in black; veins and capillaries in white; isolated spaces in yellow.

Fig. 13 Reconstruction of caudal vessels of a chick of 14 mm., Series 17. X 150. Antro-lateral view; arteries black; veins and capillaries white; lymphatic plexus connected with veins, green. The disconnected mesenchymal spaces have been omitted from this reconstruction.

Fig. 14 Reconstruction of caudal vessels of a chick of 15 mm. Series 16. X 150. Antro-lateral view; arteries black; veins and capillaries white; lymphatics connected with veins, green; mesenchymal spaces yellow.

Figure 12 9b, Lateral branches of coccygeal vein

3, Coccygeal vein draining lymphatics only

4, Coccygeal artery ^^' Lymphatic plexus connected with 8, Mesenchymal spaces (green) *^^ ^^^^« ^S^^^^^

,9, Lateral branches coccygeal veins ^^' Postcardinal veins draining haemal capillaries

Figure 14


^ 3, Coccygeal vein

3, Coccygeal vein 4, Coccygeal artery

4, Coccygeal artery 8, Disconnected mesenchymal space

5, Haemal capillary plexus 9, Lateral branch of coccygeal vein .9, Lateral branches of coccygeal vein 10, Lymphatic plexus connected with

9u, Lateral branches of coccygeal veins veins draining haemal capillaries and lym- 11, Aorta phatics 18, Postcardinal vein


As this investigation has been concerned solely with the origin of the lymphatic plexus which later forms the lymph heart, the later history of the lymph heart has not been studied. A cursor}^ examination of a 16, 16.5, 17 and 18 mm. embryo would indicate that the conclusions of Sala are in. the main correct, and that the plexus coalesces to form the single cavity of the lymph heart. The formation of the musculature, valves and the number of venous taps in the stages later than 15 mm. has not been studied.

General Discussion

Of the previous investigators of the posterior lymph heart in the chick, Sala (1) and Mierzejewski (2) have not committed themselves as to the origin of the lymphatic endothelium, while E. R. and E. L. Clark hold that the lymphatics are outgrowths from the veins and that the endothelium is specific. E. R. and E. L. Clark (5) have studied the growth of the lymphatic plexus in the living chick under the binocular microscope, using the stagnant blood backed up in the growing lymphatics from the veins as the index to lymphatic growth. To quote from their paper:

Since stagnant blood in the interior of the lymphatics is the index on which these studies are based, it was important to determine whether the blood always fi.lls the lymphatics to their tips. This was tested in two ways, by pressure over the part filled with blood to see if it could be forced farther; and by injection. As a result of numerous tests by both of these methods it was found that in these early stages, practically all of the lymphatics, save very fine connections are filled with blood. * * * * Hence, since the blood fills the successive extensions of the lymphatic as soon as formed, the use of the stagnant blood as an index for the study of lymphatic development is justifiable (p. 255).

This method has overlooked even the possibility of the presence of disconnected mesenchymal spaces entering into the formation of this lymphatic plexus. How, extravasation excepted, could pressure over the blood-filled plexus or injections into it, reveal disconnected lymphatic anlagen in the form of blind spaces in the mesenchyme? It is" obviously impossible to detect small mesenchymal spaces filled with colorless lymph by examining a living chick under the binocular microscope. The tests just described would serve to show that the blood fills the lymphatics to their tips only in so far as they formed a continuous channel connected with the veins, and would utterly fail to reveal any disconnected anlagen in the form of independent mesenchymal spaces. The appearance of a centrifugal outgrowth of the lymphatic plexus from the veins is simulated if stagnant blood or any other form of injection be used as an index to the lymphatic develop ;nent, for the mesenchymal spaces lying next to veins are the first to make the venous connection and fill with blood backed up from the general circulation. Then the spaces a little more distal join the spaces already connected, in turn are filled with blood, and so on until the entire blood-filled lymphatic plexus is formed. Thus, while the development is proceeding by the centripetal addition of disconnected anlagen, the stagnant blood in the plexus is extending in a centrifugal direction. In discussing the blood-contents of the early lymphatic plexus, which later forms the posterior lymph heart, the active haemopoesis in the surrounding mesenchyme is the only factor of morphological and genetic significance. The accidental or normal backing up of circulating blood into the lymphatic plexus, after it has secondarily established a connection with the veins, is of no significance as far as the genesis of the lymphatic structures is concerned. But the in situ origin of blood cells from the mesenchyme and their conveyance, via the lymphatics, into the general haemal circulation is of great importance, and at once places the posterior lymph hearts in the chick in the category of haemophoric lymphatics, such as are met with in the thoracic duct of the same form and in other vertebrates in various degrees of development, as has been brought out in Huntington's paper of July 1914 (10).

Until it can be absolutely proven by some other method than that of injection that all lymphatic development is centrifugal growth in continuity, with invariable continuity of lumen as well, such methods as this will seem to beg the question ; for the}^ can afford evidence only of the degree of the centrifugal extension of the lymphatics and by no means serve as a test of the process bj^ which this extension is effected once the question of annexation of mesenchymal spaces has been raised. They serve simply as a measure of the process and do not indicate its nature.

It may be argued that the spaces here described are due to the action of fixing fluids. But if this were so they certainly would not appear only in the region of the embryo in which the lymphatics are developing, and only during the short period of embryonic history during which the lymphatic vessels are formed nor would the border cells of an artefact be flattened to form endothelium. That the spaces exist in the fixed and sectioned embryos, is clearly shown in the accompanying photomicrographs, and it is safe to conclude that they exist in the living embryo as well.

But, is there any evidence that the venous endothelium does not invade this vacuolized tissue and grow out to line these independent spaces? There is: The spaces are in the younger embryos (10.5 mm.) bounded by mesenchyme cells, but as the embryo becomes larger and the spaces increase in size the bounding cells become flattened and gradations between mesenchymal cell and endothelial cell are found bounding the spaces (fig. 9, S). Nor is there ever found an endothelial tube within the flattened cells. The idea just discussed has been suggested by Knower (14) without, so far as the writer is aware, the slightest objective evidence in its support. The spaces form and acquire a venous connection so rapidly that in only a few cases are isolated spaces found bounded by fully developed endothelial cells, which are disconnected with any preexisting endothelium. But many spaces are found surrounded more or less completely by endothelium and in the remainder of their periphery b}" cells ranging from umnodifled mesenchyme to almost typical endothelial cells.

Mesothelium has been produced experimentally from connective tissue, by introducing the factors of pressure and friction, bj^ W. G. Clark (15). He has used non-irritating solid and fluid foreign bodies; celloidin and paraffin, injected into the cornea and subcutaneous tissue, and nnicus which was allowed to flow throuj2;h a fistula. He concludes that "the fact that connecti\-e tissue cells are changed in form bj^ physical agents into flat closely disposed cells, the outline of which may be defined by silver salts makes tenable the conclusion that the exposed connective tissue cells * * '^ ' may become flattened by pressure or friction or both." Therefore, mesothelimn and endothelium, both being tissues of mesenchymal origin, owe their production to identical mechanical factors.

To summaiize: The evidence found from the study of injected embryos indicates that the lymphatic plexus which later enters into the formation of the posterior lymph heart, arises by the confluence of independent mesenchymal spaces which connect secondarily with the veins; that these spaces are bounded at first by mesenchymal cells which later become flattened to form an endothelium and that both in the endothelial lymphatic walls and the adjacent mesenchj'-me an active haemopoesis, the products of which reach the general circulation via the lymphatic plexus, is taking place.

In conclusion, I wish to thank Professor McC lure and Professor Huntington wdio have directed this w^ork for their constant guidance and criticism; Professor Schulte and Professor Miller for many valuable suggestions; Dr. McWhorter for the care that he has ex])ended on the microphotographs, and Mr. Petersen for his drawings of the very complex reconstructions.

Bibliography

In the order in wliich the articles are mentioned in this paper.

(Ij Sala, L. 1900 Richerche fatta nel Lab. di Anat., Norm della R. Univ. di Roma, vol. 7, p. 263.

(2j ^NIiERzEiEVPSKi, L. 1909 Beitrag zur Entwicklung des Lymphgefiisssystems der Vogel. Bulletin de I'Academie des Sciences de Cracovie, Juillet.

(3) Stromsten, F. a. (1) 1910 A contribution to the anatomy and development of the posterior lymph hearts in turtles. Publication No. 132 of the Carnegie Institution of Washington, pp. 77-87. (2) 1911 On the relation between the mesenchyme spaces and the development of the posterior lymph hearts of turtles. Anat. Rec. vol. 5, no. 4, April.

(4) Clark, E. L. 1912 Genei-al observations on early superficial lymphatics in living chick embryos. Anat. Rec, vol. 6, no. 6, June, p. 247.

(5) Clark, E. R., and Clark, E. L. 1912 Observations on the development

of the earliest lymphatics in the region of the posterior lymph heart in living chick embryos. Anat. Rec. vol. 6, June, p. 253. (G) Miller, A. M. 1913 (1) Haemorphic function of the thoracic duct in the chick. Science, new series, vol. 37, no. 962, June, p. 879. (2) 1913 Histogenesis and morphogenesis of the thoracic duct in the chick: Development of the blood cells and their passage to the blood stream via the thoracic duct. Am. Jour. Anat., vol. 15, no. 2, September.

(7) Federowicz, S. 1913 Untersuchung uber die Entwickelung der Lymi)li gefasse bie Anurenlarven. Bulletin de 1' Acad, des Sciences de Cracovie. Series B, Juin, pp. 290-297.

(8) Allen. W. F. 1913 Studies on the development of the veno lymphatics in the tail region ot Polistotrema Stouti : First communication. Quart. Jour. Microsc. Science, vol. 59, Part 2, July.

(9) Huntington, G. S., and McClure, C. F. W. 1910 The anatomy and development of the jugular lymph sacs in the domestic cat. Amer. Jour. Anat., vol. 10.

(10) Huntington, G. S. (1) 1914 The genetic relations of lymphatic and haemal vascular channels in the embryos of amniotes. Proceedings Am. Assn. Anat., Thirtieth Session, Anat. Rec, vol. 8, no. 2, February. (2) 1914 The development of the mammalian jugular lymph sac, of the tributary primitive ulnar lymphatic and of the thoracic ducts from the viewpoint of recent investigations of vertebrate lymphatic ontogeny, together with a consideration of the genetic relations of lymphatic and haemal vascular channel in the embryos of amniotes. Am. Jour. Anat., vol. 16, no. 3, Jul}'.

(11) McWhorter, J. E., and Whipple, A. O. 1912 The development of the blastoderm chick in vitro. Anat. Rec, vol. 6, no. 3.

(12) Clark, E. R. 1914 On certain morphological and staining character istics of the nuclei of lymphatic and blood vascular endothelium and of mesench\^ne cells in chick embryos. Proceedings Am. Assn. Anat., Thirtieth Session. Anat. Rec, vol. 8, no. 2, February.

(13) Dantschakoff, Wera 1908 (1) Untersuchung fiber die Entwicklung des Blutes und Bindgewebes bei den Vogeln. Anatomische Hefte, B. 37., p. 471.

(14) Knower, H. McE. 1914 A comparative study of the embryonic blood vessels and Ijonphatics in amphibia. Proceedings Am. Assn. Anat., Thirtieth Session, Anat. Rec, vol. 8, no. 2, February.

(15) Clark, W. G. 1914 Experimental mesothelium. Proceedings Am. Assn. Anat.. Thirtieth Session, Anat. Record, February, pp. 95-96.



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