Paper - The genetic interpretation of the development of the mammalian lymphatic system (1908)
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Huntington GS. The genetic interpretation of the development of the mammalian lymphatic system. (1908) Anat. Rec. 2: 19-45.
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The Genetic Interpretation of the Development of the Mammalian Lymphatic System
By George S. Huntington
From the Anatomical Laboratory of Columbia University.
With Ten Figures.
Modern investigations of the development of the mammalian lymphatic system have led different observers to agi-ee on certain main facts, while in other important details these researches have produced more or less radically divergent views as to the |)rimary derivation of the main lymphatic vessels of the adult.
The chief contributions to this subject in recent years have been made by Sabin/ of Johns Hopkins University; by Lewis,^ of Harvard University, and by McClure, of Princeton University, and myself jointly.^ These papers deal with lymphatic development in the mammalian embryo, Sabin working on the pig, Lewis chiefly on rabbits, Huntington and McClure on the cat.
^Frederick T. Lewis. "The Development of tho Lymphatic System in Rabbits," Am. Jour, of Amit.. Vol. V, 1905, pp. 9-5-111.
Huntington GS. and McClure CFW. Development of postcava and tributaries in the domestic cat. (1907) Anat. Rec. 3: 20-32.
"George II. Huntington and C. F. W. McClure. "The Development of the Main Lymph Channels of the Cat in their Relations to the Venous Sj-stem." Am. .Tour, of Anat.. Vol. VI. 1907. Abstract in Anat. Record. Vol. I. pp. 3*141.
^Luigi Sala. "Ricerche fatte nel Laboratorio di Anatomia Xormale della R. Universita di Roma, Vol. VII, pp. 2(;;5-2(;9, April. 1900.
Of contributions which have appeared within the decade dealing with the development of the lymphatic system in vertebrates other than mammalia, the important paper of Sala* is to be especially noted, in which he describes the development of the lymphatic hearts and the thoracic ducts in the chick embryo. Tlie main views regarding the general question of mammalian lymphatic development expressed by these writers may be summarized as follows:
1. Continuous centrifugal growth of the lymphatic system from a number of outgrowths or "buds," derived directly from the venous system and retaining from the beginning their primary connection with the veins, (Sabin.)
Professor Sabin regards the entire lymphatic system as arising from four (or more^) primary centers which arise as "out-buds" from the eroibryonal veins of the cervical and inguinal regions, pervade the entire body by a process of continuous growth toward the periphery, deriving their intimal lining from the venous endothelium, with which they remain in uninterrupted connection, and following the course of the blood channels, which precede them in invading new territory.
The anterior pair of buds form the jugular lymph sacs or anterior or cervical "lymph hearts." They retain from the beginning their primary connections with the veins, and these serve as the permanent portals of entry of the adult lymphatic into the venous system. Sabin's "posterior buds" or "posterior lymph hearts" must in later stages give up their connection with the veins of the inguinal region, since such connections no longer appear in the adult mammal.
2. Direct transformation of certain embryonal veins into permanent lymphatic channels. (Lewis.)
F. T. Lewis has supported the view that the lymphatic system is directly derived from the embryonal veins, multiple detached elements of the latter becoming confluent and establishing the permanent systemic lymphatics, which then make secondary connections with the permanent venous channels. This hypothesis regards the entire adult lymphatic system as directly derived from the embryonal venous channels, certain veins or portions thereof being directly transformed into definite lymphatic vessels.
3. McClure, of Princeton, and the writer jointly advanced the view, at the twenty-second session of the Association of American Anatomists, New York City, 1907, that the main systemic lymphatic tnmks arise as independent spaces, situated without the intimal lining of the bilateral symmetrical redundant embryonal venous channels, and that these spaces, forming by confluence the permanent chief lymphatic \essels of the adult, subsequently effect a secondary connection with the definite venous system. Our observations were made exclusively on embryos of the domestic cat and in close connection with a preceding exhaustive study of the development of the systemic veins in this form find of the venous variations encountered in a large series of adult animals. These studies revealed the correlations existing, both ontogenetically and in the adult, in the venous and lymphatic organization, and the mutual interdependence of these two vascular systems, since embryonal venous channels, undergoing atrophy, afford the greater opportunity for the development of lymphatic trunks, which encroach on the territory formerly occupied exclusively by the embryonal veins of the earlier stages, or even entirely replace the latter. The developmental shifting of the primitive redundant embryonal venous system from the original bilateral symmetrical type to the dextro-venous condition of the adult, through the establishment of the innominate, azygos and iliac cross anastomoses, favors the > sinistral development of the main lymphatic channels, which replace the atrophied left segments of the primitive bilateral symmetrical venous system of the earlier embryonal stages.
^Recent discussion during Lymplintic Syniposinni of Twenty-third Session Assoc. Am. Anat., Cliioago, Jannnry l-Pt. irM'S. This nninher of tlio Anatomical Recokd, page 4G.
4. Sala's thorough work on the development of the lymphatic hearts and thoracic ducts in the chick, which will be analyzed more in detail presently, establishes in this bird the embryonal existence of a pair of posterior lymph hearts, developed directly from the lateral branches of the first five coccygeal veins. These lymph hearts subsequently make secondary connections with the general lymphatics of the body, formed by the confluence of independently developed spaces, "excavated in the mesenchyme." The lymphatic system, thus constituted from a double anlage, makes anteriorly secondary connections with the precaval veins, while the posterior lymph hearts retrograde shortly after the period of incubation is completed and disappear entirely during the first thirty or forty days of free life.
'G. S. Huntington and C. F. W. McClure. "Development of Postcava and Tributaries in the Domestic Cat," Am. Jour, of Anat, Vol. VI, No. 3, April 1, 1907. abstract, Anat. Record, Vol. I, p. 29; "The Interpretation of Variations of the Postcava and Tributaries of the Adult Cat, based on their Development," Am. Jour, of Anat.. Vol. VI, No. 3, April 1, 1907, abstract, Anat. Record. A'ol. I, p. 33. William Darrach, "Variations of the Postcava and its Tributaries in 605 examples of the Domestic Cat," Am. Jour, of Anat., Vol. VI, No. 3, April 1, 1907, abstract, Anat. Record. Vol. I, p. 30.
It is manifest that the attention of investigators of the development of the lymphatic system has been attracted to the following tliree general elements, and that they have assigned different relative values to these in their interpretations of the genesis of the lymphatic system as a whole:
- Lymphatic elements directly derived from the embryonal venous system. In their full development these organs function as the contractile lymph hearts of the lower vertebrates, while they are represented in the higher forms by temporary embryonal and highly modified adult homologous structures.
- The development of the main systemic lymphatic vessels, by confluence of multiple separate anlages, either directly derived from the emlDryonal veins or formed independently of the latter, but closely associated with the redundant eml)ryonal venous channels.
- The development and structure of the adult connections between the venous and the lymphatic system.
Of these factors the second is the most important, i. e., the development of the isolated spaces which by subsequent union form the main lymphatic channels, whether they arise as independent formations or are to be regarded as being directly derived from the venous system. Their existence contradicts the assumption of a continuous growth of the lymphatics from venous centers toward the periphery, as assumed in Sabin's conception of lymphatic development.
The existence of a direct venous derivative in the development of the mammalian lymphatic system, as the cervical or jugular lymph sac or "anterior" lymph heart, may be regarded as firmly established. The development of this structure in the embryos of the domestic cat, as determined in detail by McClure and myself, is described in a separate communication in this issue of the Eecoed. I regard the jugular sacs and the terminal parts of some of their main tributary components (as the proximal end of tlie thoracic duct) as representing in the basic plan of the entire hnnphatic system a segment interposed between the definite adult venous system and the main systemic h-mphatics, developed by confluences of lymphatic spaces, associated with embryonal veins. These spaces form the 'ke^Tiote in the correct interpretation of vertebrate lymphatic development. Sala regards them as "excavations in the mesenchyme," and in the district which he assigns to the avian thoracic ducts, as the result of canalization of originally solid cords of modified pr?e-aortic mesench^Tiial tissue.
Lewis inclines to consider them in general as detached and isolated portions of the venous system, but is somewliat indefinite in assigning to them a distinct genetic history and in deriving them directly from the venous channels, as primary veins which are subsequently directly transferred bodily to the lymphatic system.
The writer, as outlined in the preliminary communication published last year, believes that these spaces are formed along the embryonal veins, without their intimal lining, and that they are largely determined in their development by the atrophy of certain of the original embr)'onal venous pathways which they secondarily replace.
If in the final adult organization the systematic lymphatic channels, formed by fusion of the discrete extra-venous spaces, communicate with the general venous system, it can only be accomplished by the interpolation of the jugular lymph sacs, they constituting a link, which in the mammal unites two genetically separate sets of vascular channels at definite and — within normal limits of variation — constant points.
It is evident that any interpretation of lymphatic development in the mammal must be based not only upon careful observations of the ontogeny of the lymphatic system in any one individual form, but upon the phylogenetic history of the lymphatic system as a whole, and upon the adult conditions encountered in mammals, as well as in vertebrates lower in the zoological scale.
If the hypothesis above outlined in reference to the genetic interpretation of the development of the lymphatic system and its association with the venous system in the mammalian embryo is true, then all known facts, both of phylogenetic and ontogenetic development of the lymphatic system, should conform strictly to the morphological demands made by the same. It is the purpose of this communication to bring together — as far as possible — the observations and facts which form the basis of this conception of mammalian lymphatic development, without considering the details of structure, which are reserved for a subsequent and more complete publication.
We can arrange the subject matter under the following headings:
I. Summary of observations on the development of the jugular lymph sacs and the general lymphatic system in embrvos of Felis domestica.
II. Phylogeny of the lymph hearts and of homologous structures in the vertebrate series.
III. Ontogeny of the mammalian jugular lymph sacs as compared with the embryonal avian lymph hearts described by Sala, and general comparison of avian and mammalian lymphatic development.
1. Summary of Observation on the Development or the Jugular Lymph Sacs and of the General Lymphatic System in Embryos of Felis Domestica
1. The jugular lymph sacs in the embryo of the cat are direct derivatives from the early redundant embryonal venous pathways of the preand post-cardinal regions, adjacent to and including their point of confluence to form the duct of Cuvier.
They subsequently — voiding their early blood contents — become, as far as it has been possible to accurately determine, for a time entirely separated from the venous channels from which they arose in the manner described in detail in another communication. Subsequently they form secondary connections with the venous system, at definite points, and with the general systemic lymphatic vessels.
2. The independently formed isolated spaces, which develop along th-i course of the embryonal veins, and which, becoming confluent, constitute the anlages of the main systematic lymphatic channels.
In the present state of our knowledge regarding the development of the mammalian lymphatic system, the appearance of these isolated spaces constitutes one of the most important phases of the entire problem. These spaces, developing along the course of the principal venous channels, become later confluent with each other to form the principal systemic lymphatic channels, which gain their permanent entrance into the venous system through secondary connections established with the jugular lymph sacs or lymph hearts.
Three main possibilities suggest themselves in reference to the genesis of these spaces:
A. Either they are detached and evacuated portions of the primitive embryonal venous system, which, after losing their blood contents, became confluent to form larger spaces. In other words, they represent multiple rudimentary lymph heart formations, developed in the same manner, directly from the venous system, as the jugular lymph sacs.
B. Or those spaces are formed independently outside the lumen of the embryonal veins, in the sense previously defined.
C. Or, lastly, there is a combination of these two processes, namely, lymph heart formation at a number of points along the course of embryonal veins (mesenteric, inguinal, etc.), in addition to the main jugular lymph sac, with the formation of intervening lymphatic channels resulting from the confluence of independently formed spaces.
Against the first hypothesis is the uniform character and appearance of these spaces in their relation to the embryonal venous channels, and the fact that up to the present definite and constant connections between these spaces and the vascular system have not been demonstrated. Also that they are uniformly and from their earliest inception empty and void of blood contents, entirely differing in their structure and their relations to the venous system from the early veno-lymphatic stages of the jugular lymph sac elements.
In favor of the first and of the third hypothesis is the phylogenetic history of multiple lymph heart derivatives from the embryonal venous system.
As far as I have been able to accurately determine by careful study of numerous serial sections and plastic reconstructions of the embryo of the cat in the important stages, the general systemic lymphatic vessels, as distinguished from the jugular lymph sacs, arise, not by direct transformation of veins, but by the formation of spaces lying outside the intimal lining of the veins, which spaces, becoming confluent, form the general lymphatic channels of the body. They are closely correlated to the main and secondary venous channels, but independent of the same, except in as far as abandoned and atrophied embryonal venous pathways afford to the lymphatic vessels the opportunity for more extensive development, and permit them to secondarily occupy the area of the shrinking vein.
I have been unable to obtain any evidence that the lymphatic spaces, developing along the course of the principal embryonal venous channels, outside the jugular lymph sac area, have been directly derived from the veins with which they are so closely associated. Nor have I been able to establish at any point direct and indisputable connections, primary or secondary, between these spaces and the embryonic veins which they accompan3\ The peripheral general lymphatic channels appear to be developed by confluence of spaces independent of the venous system, althought closely associated with the same. The histological picture presented by ' them differs radically from that of the jugular veno-lymphatic derivatives. They begin as minute extra-venous vacuoles, closely applied to the surface of the veins which they accompany. They enlarge as the lumen of the vein diminishes. They become confluent with each other, but they never, from their first inception, contain red blood cells, nor do they, as far as I have been able to ascertain in numerous carefully studied series of excellent preservation and fixation, communicate with the blood channels. In the present state of our knowledge of the genetic history of these spaces, I helieve we are obliged to consider them as developing independently of the venous system, in the sense that they are not direct derivatives from the embryonal veins, but lymph spaces formed outside of the lumen of the venous channels.
3. Finally, after the establishment of connections between the jugular lymph sacs (venous in origin) and the general systemic lymphatic vessels (developed along the embryonal veins by confluence of extravascular spaces), the combined and now continuous and definite lymphatic system establishes, in the mammalian embryo, its permanent points of entry into the venous system.
I am convinced that the definite adult connections of the venous and lymphatic systems are secondarily developed, although they occur normally at definite points, which, in the embryo of the cat, correspond to two of the primitive connections of the jugular lymph sac with the embryonal venous channels. These points are:
A. The angle of confluence of the common jugular vein, i. e., of the combined trunk of the external jugular and cephalic veins with the internal jugular vein (cephalic lymphatico-venous tap, corresponding to the primitive junction of the ventral division of the veno-lymphatic sinus with the precardinal vein at its junction with the jugular promontory).'^
B. Jugulo-subclavian angle (caudal lymphatico-venous tap, corresponding to the primitive junction of the dorsal division of the venolymphatic sinus with the jugular promontory at the entrance of the primitive ulnar vein).'^
The steps by which this irruption of the completed lymphatic system into the definitely organized venous system of the mammal is accomplished are so regular, so typical in their development and present such constant and consistent pictures that, once recognized, they stamp the final lymphatico-venous connection as a secondary process, marking the establishment of permanent adult conditions.
"We have, therefore, in order to accentuate the intermediate position of the jugular lymph sacs, described their initial organization as constituting the veno-lymphatic stage in the upbuilding of the entire lymphatic system.
'For details and explanation of descriptive terms cf. .ioint paper of MoClure and writer on the Development of the Jugular Lymph Sac in this number of the Record, p. 1.
The conception of tlie development of this system in the manimal, which has impressed itself on me as combining all definitely ascertained facts into a logical and congruent whole, may be summed up as follows :
1. Development of the veno-lymphatic sinuses and the resulting jugular lymph hearts directly from a definite portion of the pre- and post-cardinal veins.
2. Evacuation of the blood contents of the veno-lymphatic sinuses through certain of their primitive connections into the j)ermanent venous channels.
3. Subsequent complete separation of the voided veno-lymphatic sinuses from the veins which gave origin to tbciii.
4. Development of extra-venous spaces along the course of the main embryonal veins, and confluence of these spaces to establish the systemic lymphatic channels su^bsequently destined to form secondary connections with the jugular lymph sacs.
5. Secondary connection of the two elements entering into the composition of the definite lymphatic system, viz : the d(>tached and emptied veno-lymphatic sacs or anterior lymph hearts, originally derive<l from the veins, and the general systemic lymphatic channels, formed from the beginning independently of the veins, but closely correlated to them.
6. Final entrance of the completed lymphatic system, thus formed from a double anlage, into the permanent venous system by the formation of the typical secondary connections, with their characteristic wedge-shaped entrance and annular valves.
There are two points which deserve mention in outlining this genetic interpretation of mammalian lymphatic development :
1. It is quite possible, in fact -probable, that in the mammal, in addition to the more fully developed jugular lymph sac, or "anterior lymph heart," other more rudimentary direct venous derivatives of the lymphatic system occur further caudad, possessing exactly the same significance and to be interpreted as incomplete lymph heart formations, which may or may not be multiple. Phylogenetically this would be expected, although from the evidence at present available these structures appear to be much more reduced and rudimentary than the anterior or jugular lymph sacs. They are incomplete in the sense that in the mammal, after complete organization of the venous and lymphatic systems has been accomplished, they no longer serve, as do the jugular lymph sacs, as portals of definite lymphatico-venous connections. Thus Baetjer's mesenteric sac and Sabin's caudal lymph heart may very well represent in the general mammalian plan reduced and rudimentary lymph heart formations of direct venous origin, as will be more fully considered presently in dealing with the phylogenetic aspect of lymph heart development. iVt present it is sufficient to point out that the interpretation of mammalian lymphatic development given above admits of. the ontogenetic appearance of multiple direct venous derivatives of the primitive lymphatic system, representing incomplete lymphatic heart elements, only differing from the more highly developed anterior or jugular lymph sacs or lymph hearts in that they do not persist as permanent links between the lymphatic and venous systems of the adult, as do the homologous and more complete jugular structures.
2. The question of peripheral lymphatic growth is not involved in formulating the basic ground plan of development of the lymphatic system. When that system is once established and has acquired structural fixity, further growth of the lymphatic channels will be by continuous peripheral extension, entirely homologous to the similar enlargement of blood vascular areas, whether occurring normally during development or pathologically after normal growth is completed.
II. Phylogeny of the Lymph Hearts and of Homologous Structures IN the Vertebrate Series
The vertebrate lymphatic system, both in its phylogeny and in its embryonal development, reveals a compound character, the two component elements being the lymphatic hearts and the general systemic lymphatic vessels. Phylogenetically the most striking character is found in the gradual numerical reduction, degeneration and ultimate almost complete elimination of the lymphatic hearts, correlated, in Mammalia, with high development of the systemic lymphatic vessels.
The lymph hearts of the fishes are apparently represented by the lymphatic sinuses found on each side in the scapular region, in direct communication with the venous system and receiving the lymphatic vessels of the head and body. They appear to constitute early phylogenetic types of lymph heart formation, before the walls have developed striped muscular tissue.
In some forms (Silurus, Angnilla) rhythmically contractile lymph hearts develop in the caudal region.
The lymph hearts reach their highest development in the Amphibia, with striated muscular fibers forming part of the walls.
In the Urodeles as many as 14-20 of these organs exist on either side of the trunk and tail at the junction of the dorsal and ventral trunk musculature. A lymphatic sinus included in the walls of the Truncus arteriosus of these forms has been described as a "central lymph heart."
In Anura the number of lymph hearts is reduced to two pairs, cephalic and caudal, the former placed between the transverse processes of the third and fourth vertebra, the latter between the urostyle and pelvis.
From this point on the Sauropsid branch, including reptiles and birds, appears to have specialized on the posterior or caudal organ to the practical exclusion of the anterior or cephalic lymph heart, except in as far as rudiments of this structure may be represented in the anterior or jugular lymphatico-venous connections in these vertebrate classes.
In Eeptilia only the posterior of the two pairs is retained in the adult organization, situated at the junction of trunk and tail, on the vertebral transverse processes or on the ribs of this region.
The posterior lymph hearts appear during the embryonal period in birds at the boundary between the sacral and coccygeal vertebrse, partly covered by the M. coccygeus dorsalis, and in open communication with the coccygeal and pelvic veins. In the chick they are evidently functionally active during the period of incubation. They undergo rapid degeneration after free life is established and subsequently (30-40 days) disappear entirely.
In some other avian species they persist in a more or less modified condition in adult life.
In some forms they appear well developed : in still others they present themselves as rudimentary organs, forming simple vesicular dilatations; in still others, as in the chick and in all Gallinacege, they appear to be uniformly wanting in the adult.
In birds the anterior lymph heart apparently no longer develops completely. From the account given by Sala it appears, however, extremely probable that in a rudimentary form it unites the precaval veins with the independently established systemic lymphatic channels (cf. infra).
In Mammalia, on the other hand, in contradistinction to the posterior Sauropsid type, lymphatic heart development is centred, at least chiefly, in the anterior region. The early embryonal veno-lymphatic sinuses and the subsequent jugular lymph sacs must from their ontogenetic history be homologized with the more completely developed lymph hearts of the lower vertebrates, althou2:h thev are hi2:hlv modified, relatively much reduced, aiid no longer develop muscular fibers as a constituent of their walls.
Professor Sabin has described an anterior cervical and posterior inguinal organ in pig embryos.
At the twenty-third session of the Association of American Anatomists, held in Chicago, January 1, 2 and 3, 1908, W. A. Baetjer, of Johns Hopkins University, presented, through Sabin, a paper "On the Origin of the Mesenteric Sac and its Eelation to the Thoracic Duct,"^ the details of which are at this writing not yet published. Presumably this mesenteric lymph sac represents the anlage of the mammalian receptaculum chyli.
In the studies made jointly by McClure and myself on cat embryos we have traced the development of the anterior or jugular lymph sac in detail. In the cat, as far as our observations extend, no correspondent formation occurs in the posterior end of the embryo, although certain stages in the veno-lymphatic development caudad of the omphalomesenteric artery and the subcardinal cross anastomosis strongly suggest foreshortened and rudimentary ontogenetic processes, homologous to those observed in the more complete development of the jugular lymph sacs. More detailed investigations and carefully executed plastic reconstructions are needed to clear up this question, but, as previously stated, multiple rudimentary lymph heart formations may be expected in the mammalian embryo as being in line with the phylogenetic history of these organs. If they exist, as seems probable, they no longer function as ports of entry of the lymphatic into the venous system. As far as present evidence goes, they become, when once detached from the venous system, incorporated in the general lymphatic system.
Eeviewing the facts at present established, it is fair to state that the lymph hearts in their highest development (amphibia, reptiles and during inculcation in birds) are derived primarily from the venous system, retain their connections with the same and receive the systemic hmiphatic trunks of the body.
No matter what their number or situation may be in individual vertebrate forms, they are closed sacs, with striped muscular tissue entering into the composition of their walls, interposed between the general systemic lymphatic trunks and the permanent venous system. They thus occupy the position of intermediate elements, originally venous in derivation, but specially modified and transferred to the lymphatic system, their original points of connection with the venous system constituting permanent portals of lymphatico- venous entry in amphibia and reptiles, and functioning as such during the embryonal period in birds. They evidently act as contractile reservoirs, receiving the centripetal flow of lymph from the general systemic and peripheral lymphatics. By virtue of their muscular contractility they are able to empty the lymphatic fluid accumulated in their cavity into the venous system through the original avenues of connection with the same, the direction of the flow being apparently regrilated by definite valve formation in the interior of the sacs and the connecting vessels.
^Tbis uumber of the Anatomical Record, page 55.
As a secondary function it is possible that they may promote the centripetal flow of lymph from the periphery foward the lymphaticovenous confluence by a pumping or suction action.
On the other hand, the anterior lymph hearts of Mammalia, the jugular or cervical lymph sacs, while no longer contractile organs, develop directly from the pre- and post-cardinal venous confluence, and subsequently, after receiving the terminals of the general lymphatic system, form, by secondary connection, the link of communication between the lymphatics and the permanent veins.
Begarded, therefore, from the general standpoint, the lymphatic hearts and the systemic lymphatic vessels present throughout the entire vertebrate series a uniform and consistent structural picture, wliose main features may be summarized as follows:
1. Lymphatic Hearts. — They develop directly from embryonal venous channels.
They are always placed at the points of communication between the lymphatic and the venous systems, interposed between the two and communicating with both. ^
In the lower vertebrate classes these organs develop contractile walls, are multiple, and maintain numerous points of connection witli the venous system throughout adult life (some Fishes, Urodeles). In ascending the zoological scale they become reduced numerically to two pairs, cephalic and caudal (Anures). Progressive phylogenetic development (Eeptilia) shows reduction of the anterior or cephalic pair, while the posterior organs persist and retain throughout adult life their original structural character and function as true lymph hearts.
In birds the reptilian type appears ontogenetically as the caudal lymph heart, well developed and evidently functionally active during the period of incubation, but lost in most forms in the adult condition.
It is quite probable that a reduced and rudimentary anterior lymph heart forms in birds the uniting link between the venous and lymphatic system (cf. infra analysis of Sala's description of anterior lymphaticoprsecaval junction).
In Mammalia finally the progressive- development of the general systemic lymphatic system is correlated to the reduction and almost complete elimination of the posterior lymph hearts (inguinal, mesenteric) vi^hich may appear during certain ontogenetic stages, as incomplete structures, but are not retained as final and definite lymphaticovenous adult connections. The anterior lymph hearts, on the other hand, modified in structure as the jugular or cervical lymph sacs, develop more completely and serve as the links of secondary connection between the lymphatic and the venous system.
2. The General Systemic Lymphatic Channels. — These develop either as direct derivatives of the embryonal venous system (Lewis) or as spaces formed independently of the veins, although closely associated with them in the sense previously defined (Huntington).
They establish secondary connections with the lymphatic hearts or their reduced mammalian homologues, the jugular lymph sacs, and through these organs form their permanent connection with the venous system. In lower vertebrate types, where the lymph hearts are numerous, the general systemic lymphatics are more simply organized and less extensively developed as a continuous system. With the reduction of the lymph hearts in ascending the zoological scale the systemic lymphatic system assumes a more and more important position and overshadows in extent and complexity the primitive multiple lymph heart formation.
3. In the higher forms the latter is reduced, but of necessity retained, in at least one of its primordial districts, as affording the portal of lymphatico-venous connection.
The single or double lymphatico-venous entry of the mammal thus stands in contrast with the multiple connections of the Urodele amphibian, but is correlated to the same by the difference in the type of development exhibited by the two primary components of the lymphatic system, viz: the lymph hearts and the systemic lymph channels.
4. The lymphatico-venous junction trends phylogene'tically toward the confluence of the main embryonal venous channels, viz: the Cuvierian junction of the pre- and post-cardinal veins. Thus, in the avian lymphatic organization, in spite of the high ontogenetic development of the posterior lymph heart, the definite adult lymphatico-venoiis connection is established with the preeaval veins. In the mammal the corresponding lymph heart, as the jugular or cervical lymph sac, constitutes the only permanent link or links of communication in the adult between the lymphatic and venous systems. The multiple lymphatic hearts of the lower types have in the higher forms either disappeared altogether or have, after an evanescent ontogenetic existence, become incorporated in the general systemic lymphatic apparatus. Thus the lymphatic hearts, from the beginning of the phylogenetic series up to the highest vertebrate types, occupy, no matter how modified in form or structure, or how much reduced numerically — a constant, consistent and uniform position — as elements, directly derived from the embryonal venous channels, interposed between the system of the general lymphatics and that of the permanent veins, destined to receive the same.
These lymph heart links, joining the two great correlated divisions of the compound veno-lymphatic vascular system, may be multiple, as in the lower vertebrate types, or reduced to a single pair, as in higher forms. Their morphological position and genetic significance remain precisely the same under all modifications encountered in the entire zoological series.
III. Ontogeny of the Mammalian Jugular Lymph Sacs as Compared with the Embryonal Avian Lymph Hearts Described by Sala, and General Comparison of Avian and Mammalian Lymphatic Development
In defining the fundamental common ground plan of vertebrate lymphatic organization, as illustrated by the comparative study of avian and mammalian development, the two distinct component elements must be sharply differentiated in their mutual relation and in their connection with the venous system.
1. The Lymphatic Hearts
These, as well as their rudimentary representatives in the higher forms, are direct derivatives from the venous system. A limited number of lateral tributaries of the main venous trunks in the jugular region (mammalian embryo) and in the iliac region (avian embryo) specialize by dilatation and confluence. In the mammal, in addition, a considerable segment of the pre- and postcardinal veins, adjacent to their Cuvierian confluence, becomes separated by fenestration from the proper venous channels, and. together with the fused and dilated dorsal tributaries involved in the process, forms a capacious sac or bag, the jugular or cervical lymph sac. In the embryo of the chick a corresponding structure develops from the pelvic and coccygeal veins, becomes invested by a layer of striped muscular fibers and functions during the period of incubation as a contractile lymph heart, corresponding to the adult organs of reptiles and amphibians. In the chick, according to Sala's researches, the development of the lymphatic heart is restricted to the posterior region of the embryo. Derived from the lateral branches of the first five coccygeal veins, the lymph heart passes through a definite ontogenetic cycle, including the development of a sheath of striped muscular tissue, but is lost shortly after completion of incubation, and is not carried, at least in its original form, into the adult lymphatic organization of the bird.
The lymphatic heart development of the chick may be schematically represented in Figs. 1-5, based on Sala's description and the plates accompanying his publication.
The sacral and coccygeal veins of the chick are laid down in the first hours of the seventh day of incubation, a dorsal and a lateral branch of each segment uniting into a common trunk which opens into the caudal end of the post-cardinal vein. The lateral branches of the first five coccygeal veins of each side develop the lymphatic hearts. These veins are from the beginning larger than the succeeding veins of the same series not involved in the lymphatic heart formation. In the mesenchyme surrounding these lateral branches of the proximal five cocc3^geal veins "little spaces or fissures develop in direct connection with the veins." To quote Sala's words, "One would in fact say that these fissures are only simple dilatations and ramifications of the veins themselves."
These spaces are at first few and of irregular form, "arranged segmentally, in a linear series, parallel to the vertebral column, corresponding to the point of penetration of each venous branch into the intermuscular segment" (Fig. 1).
Later (Fig. 2) these spaces enlarge and fuse with each other, the remnants of their Avails appearing as more or less complete internal septa or diaphragmata, producing a "system of cavities, very irregular in form and dimensions, intercommunicating, and connected at the same time with the lateral branches of the first five coccygeal veins." The mesenchyme surrounding this system of cavities becomes gradually denser, differentiating from the adjacent indifferent mesenchyme. In the second half of the eighth day the walls of the primitive lymph hearts are still composed exclusively of lengthened mesenchymal cells, without trace of muscular fiber. The cells directly enclosing the cavities have flattened and have transformed themselves into endotlielial cells, while the more peripheral cells of the walls are elongated and have extensively fused with each other.
"These cavities excavated in the heart are very irreguhir in form and dimensions, divided incompletely one from the other by means oi diaphragmata or trabecule, with perforations here and there, and also composed of memsenchymal cells fused together." "The cavity as a whole may be at this stage compared to a sponge with large and small holes. Contrary to Budge, I have observed that the cavities at this time often contain red globules of blood, and sometimes appear quite filled with them." '
Muscular fibers first appear in the surrounding mesenchymal wall of the lymph heart cavity during the second half of the ninth day, scattered irregularly at first, subsequently forming a continuous stratum embracing the entire sac, for the most part in a circular iiiamicr (Fig. 4).
The lymph heart obtains its greatest development between the fourteenth and fifteenth day. The fusion of the individual cavities has continued until at this time the diaphragmata or trabecule in the interior have become much reduced in number, so that the lymphatic hearts appear as single cavities, 1.5 to 2 mm. in diameter.
"The formation of the lymph hearts . . . shows us the close connection which these organs assume with the coccygeal veins. From tlieir first appearance the cavities around which the mesenchymal cells condense and which precede the formation of the real heart, are in the last analysis nothing but terminal dilatations of the veins themselves, which have gradually grown in volume and fused together. This communication between the lymphatic hearts and tlie coccygeal veins, which appears so early, is maintained (in part) throughout the whole duration of the embryonic period, and also for that small space of adult life in which these organs persist."
As the development of the lyuipli hearts (Fig. 4) proceeds tliey lose their connection Avith the first and the last of the series of the five proximal coccygeal veins, the intermediate three veins (second, third and fourth of the original series) remaining and "leaving the heart in large apertures excavated in its walls, to correspond with which, from the twelfth day, the intimal surface of the sac forms a more or less manifest projection, sometimes circular, i. e., continuing around the aperture, at other times limited to a portion of the circumference of the aperture itself, and which corresponds probal^ly to the valvular formation noted by Budge."
2. Systemic Lymphatic System
The lymph hearts make secondary connections with the general lymphatic system relatively late, toward the end of the tenth day, one, or more rarely two, lymphatic vessels uniting the hearts with '"the lymphatic spaces which have formed in great numbers around the two hypogastric veins and their median anastomotic branch (Figs. 4 and 5).
"These spaces appear in the last hours of the ninth day. forming fissures, not very large at first and of irregular form, excavated in the mesenchyme which immediately surrounds the above mentioned venous vessels."
This picture af avian lymphatic development furnished by Sala's observations gives the following salient points :
- Formation of lymph hearts as the direct products of dilatation, modification and fusion of certain embryonal venous tributaries (Figs. 1, 2, 3).
- Eeduction in number of the primitive connections of the lymph hearts with the venous system (Fig. 4).
- Development of the general systemic lymphatic vessels, as the result of fusion and confluence of independently formed perivenous mesenchymal spaces (Figs. 4 and 5).
- Establishment of secondary connections between the lymph hearts and the independently formed general lymphatic system (Fig. 5).
- Soon after the completion of incubation regression and ultimate disappearance of the lymph hearts as specialized parts of the general lymphatic system.
Comparison of Sala's Observations with the Results Obtained in a Detailed Study of the Development of the Jugular Lymph Sacs in the Embryo of the Cat, and Correlation of the Homologous Parts of the Lymphatic System in Avian and Mnmmalian Embryos.
(Figs. 1-5 compared with Figs. 6-10.)
In the cat the development of the jugular lymph sacs represents the regressional embryonic appearance of the anterior lymph heart of lower vertebrates. This value was assigned to the structures by Sabin in her earlier publication/ and questioned later by Lewis," by reason of the absence of muscular elements in the walls of the sac. As soon, however, as the finer details in the development of the sacs were established by McClure and the writer, a comparison of the results obtained with Sala's full and accurate account of avian lymph heart development dispels all doubt as to the intrinsic character of these structures in the mammalian embryo, and puts them in line, as rudimentary representatives, with the series of more fully developed lymphatic hearts in other vertebrate classes.
Dilatation and fusion of certain precardinal tributaries (Fig. 6, 1-3 or 4), together with the separation by fenestration and confluence of a secondary channel from the dorsal segments of the pre- and postcardinal veins adjacent to and including their junction at the duct of Cnvier (blue area in Figs. 6 and 7), yields a product, the jugular lymph sac, constructed on the same principles as the coccygeal lymph heart of the chick in early stages (Figs. 1 and 2), but never attaining the degree of development in which striped muscular filers appear in its walls. The lymph sacs of the earlier mammalian stages, after confluence and fusion of the component elements (Fig. 8), show their compound nature, and the multiple interior partitions and septa betray their origin from a number of fused and confluent venous spaces, reproducing exactly the earlier avian condition described by Sala (Figs. 2 and 3).
The resulting mammalian lymph heart presents at the height of its development (Fig. 7) the appearance of a capacious sac or sinus, directly derived from the venous system, lined by an endothelium continuous with the intimal lining of the true venous channels.
In the early stages the veno-lymphatic sinns is in free communication with the pre- and post-cardinal veins by the openings of some or all of the original dorsal tributaries involved in its formation (Figs. 6, 1, 2, 3, and at times part or the whole of 4) and by secondary openings which, during the separation by fenestration from the primitive venous pathways, the dorso-lateral portions of these channels, involved in the formation of the lymph sac, have retained with the parent vein, as the persistent intervals between the fenestral spaces, which, with the more complete detachment of the veno-hnnphatic sinus, become drawn out into secondary channels^, connecting the jugular lymph sac with the permanent veins. Thus in the early stages, up to 10 mm. embryos, the yeno-lymphatic sinus, which precedes the appearance of the true lymph heart, is in free and open communication with the venous system by a number of connections (Fig. 7), just as the corresponding structure is for a much longer period in the avian embryo (cf. Figs. 2 and 3).
^Loc. cit, p. 110.
In the cat embryo the following observations were made:
Series 31. Embryo 5-6 mm. Left side. 13 communicating channels between the rudimentary veno-lymphatic sinus and the permanent veins.
Series 3. Embryo 7 mm. Left side. 9 communications.
Series 106. Embryo 9 mm. Left. 13 communications.
Series 113. Embryo 10 mm. Left side. 1-1 communications.
These early multiple connections of the sinus with the true veins are subsequently greatly reduced in number (Fig. 8), just as in the chick the original five lymph heart veins are reduced to three by the loss of the heart's connection with the first and fifth coccygeal veins (Fig. 4).
In the mammal this process of secondary separation of the lymph hearts or jugular lymph sacs from the venous channels which primarily gave origin to them, is carried much further than in the avian embryo. In the cat two of these connections are usually retained for some time after the remainder have been lost, one with the precardinal where the vessel receives the comljined trunk formed by the cephalic and external jugular veins (cephalic primitive tap. Fig. 8), the other further caudad, originally in post-cardinal territory, at the terminal of the primitive ulnar vein, becoming sul)sequently, after establishment of the subclavian vein, located at the angle of confluence of this vessel with the main jugular trunk (caudal primitive tap, Fig. 8).
Up to this point the general developmental processes in bird and mammal have been along practically parallel lines. The fact that striped muscular development does not occur in the walls of the mammalian lymph sac, but does so in the chick, suggests, as Budge has pointed out, that in the latter the posterior lymph hearts may be of functional value during the embryonal period in the lymphatic circulation. In the mammalian embryo they do not appear to have this value, but they are retained in a more rudimentary form and adapted to the complicated establishment of the secondary and final connections established between the definitely organized lymphatic and the permanent venous system.
The jugular lymph sac of the cat represents, therefore, at this stage a sac still filled with ])lood and still in communication witli the venous system at one or more point!>, the multiple early veuo-lymphatic connections having undergone considerable numerical reduction (Fig. 8). The structure corresponds, in all essential ontogenetic characters, to the conditions described by Sala for the development of the lymph heart of the chick.
From this point on the organ in mammals enters a new developmental phase, not represented, as far as definite knowledge based on actual observations is available, in the lower vertebrate classes. It is exceedingly probable, however, that further careful researches will determine the existence of a more rudimentary anterior lymph heart or jugular lymph sac in avian and reptilian embryos, and that the final entry of the lymphatic system into the prgecaval veins is, in the bird, established through the intervention of this structure, on the same general plan as exists in mammals.
In the embryo of the cat the lymphatic sac becomes much more completely separated from the venous system and very rapidly evacuates its blood contents into the latter through one or more of the primitive channels of communication. This "tap of evacuation" appears to enlarge at this time, and the process of emptying the veno-lymphati'j sinus of its blood proceeds with great rapidity.
As soon at this is accomplished the "tap of evacuation" also closes and becomes detached from the venous channels, so that the sinus now forms a closed empty sac, completely separated from the venous system from which it arose, the jugular lymph sac proper, as contradistinguished against the earlier veno-lvniphatic sinus or anterior Ivmph heart (Fig. 9).
It is somewhat difficult to interpret this feature in the development of the mammalian lymph sac, since the permanent normal connections of the lymphatic and the venous system take place at the identical points occupied in the preceding stage by the primitive veno-lymphatic taps which are the last to close in the temporary se])aration of the lymphatic sac from the venous system. The picture afforded by the proper stages (10.7 mm. to 12 mm.) is, however, so constant and the observations so numerous, that it seems necessary to accept this separation as occurring normally and constantly. This closed sac then forms two sets of secondary connections:
(a) With the general system of independently formed perivenous lymphatic vessels (Fig. 9).
(b) With the venous system, re-entering the same by the establishment of a com]ilicated secondary opening, guarded by a circular valve.
These secondary lymphatico-venous connections are, in the cat, made normally at two points, the angle of confluence of the internal jugular with the combined trunk of external jugular and cephalic veins (cephalic secondary tap) and at jugulo-subclavian angle (caudal secondary tap), corresponding to the points at which in the earlier stages the primitive direct connection between the veno-lymphatic sinus and the true veins were longest retained (taps of evacuation. Fig. 10). The failure in any individual to establish one or the other of these typical connections leads to the adult variations of single lymphatico-venous tap described in another paper, while the early multiple connections of the lymphatic sinus with the venous system open up a wide range of more aberrant variants, on the assumption that any of these may abnormally replace the two typical taps of evacuation and subsequently serve as the portals of definite secondary lymphatico-venous entry.
The relative size of the jugular lymph hearts or lymph sacs diminishes after the final venous connection is established, and in the later embryonal stages and in the adult they appear as rudimentary structures at the site of the veno-lymphatic entrance. In the early stages the mammalian and avian embryos agree in the development of homologous parts of the lymphatic system, the jugular lymph sac of the former corresponding to the coccygeal lymph heart of the latter. They also agree in the development of the general systemic lymphatics by confluence of independently formed spaces, and in the secondary connection between the resulting lymphatic channels and the lymph heart or its mammalian representative, the jugular lymph sac. The bird, however, retains the more fully developed contractile lymph heart unchanged until the end of incubation and for a short period after adult conditions are established, the organ then undergoing rapid degeneration and elimination. In the mammal the corresponding anterior structure is never functionally contractile, and probably never acts as a "lymph heart." It is, however, developed in a modified form and incorporated in the final secondary connection established between the lymphatic and the venous system. The adult connection of the lymphatic system witli the prscaval veins in birds is likewise a secondary formation. It is quite probable that in its establishment an extremely modified and reduced anterior lymphatic heart is interpolated, as in the mammal, between the venous and the lymphatic systems, in the service of this secondary and final connection. Sala's account in this particular is not very full or conclusive, and the subject deserves careful revision in the light of the facts ascertained in the developmental history of the mammalian jugular lymph sacs.
Sala, after describing the structures which he considers the avian thoracic ducts as being formed by the confluence of excavated spaces in "cords" of modified mesenchymal tissue, says:
"In embryos of eight days ... in that portion of its course in which the cord stands in a medial relation to the superior vena cava, betwen the latter and the arch of the corresponding Ductus Botalli, the cavities are numerous and some come into contact with the wall of the vena cava, but at this period there does not yet exist any communication between the vein and those cavities ivhich are hollowing themselves out in the cord."
And further, in describing the next stage, embryo of eight days and eighteen hours :
"In the part in which the cord is in contact with the medial wall of the vena cava superior the numerous cavities excavated in it are extended up to contact with the vein; in fact, I do not exclude the possibility of some of them being in communication with the vein itself, although I have not succeeded in fully demonstrating this connection for this period, which communication, nevertheless, is already evident at the completion of the ninth da}', as we shall see."
Speaking of the first appearance of the anlages of his "cords," he states that the first traces of these structures appear somewhat later than the lymphatic hearts, i. e., in the second half of the eighth day. Before this time, in embryos of seven days and six hours, in the region where the thoracic ducts are to be formed, no trace of such formation can be foimd. He then goes on to say:
"In the mesenchyme which surrounds the thoracic aorta and the large arterial vessels which open into this (Botallian ducts), as also in the mesenchyme which limits mesially the superior vena cava, there exist, it is true, numerous spaces or cavities, clothed with endothelium, and more or less large, of irregular form, which perhaps correspond to the lymphatic cavities of the first circulation of Budge, hxd none of these communicate with the superior vena cava."
At the middle of the eighth day, in the same mesenchyme, in addition to these spaces, are found here and there small areas in which the mesenchyme cells "present themselves much nearer to each other, so as to form little accumulations or lumps, whicli contrast clearly with the rest of the mesenchvma. Highly magnified, these accumulations appear to consist in large part of elements offering all the characteristics of young connective tissue cells of roundish form, with no projections and a large and intensely colorable nucleus. Some are in a state of karyokinesis. In the midst of these elements appear red blood globules in larger or smaller quantities." These accumulations are especially developed in the mesenchyma on the medial aspect of the superior vena cava "in correspondence with the point in which it receives the outlet of the jugular and subclavian veins."
We seem to have here, couched in different language, a description which corresponds in all essential points to the homologous stages in the mammalian embryo, up to the period of the establishment of the permanent connections l)etween the evacuated veno-lymphatic sinus and the venous system.
The early avian period, with blood contents in the aggregated "lumps" and mesenchymal spaces, seems to point to a direct venous derivative as forming part of the bird's lymphatic organization, quite corresponding to the early veno-lymphatic stages of the mammalian jugular lymph sac. Sala's account does not give a clear insight into the genetic relation of these structures to the embryonal veins, but the fact that they at one time contain blood cells suggests their direct connection with and derivation from embryonal venous pathways.
They subsequently lose their blood contents, enlarge, become confluent, approach the permanent venous channels, and finally establish a secondary connection with them. Thus Sala's account represents in every essential detail a foreshortened and abbreviated review of the genetic processes governing the development of the jugular lymph sac of the mammalian embryo.
It should also be remembered in this connection that the terminal segment of the mammalian thoracic duct is apparently a veno-lymphatic derivative in the sense defined, making subsequent secondary connections with the independently formed extra-venous portions of the canal in the supra-cardinal venous area, just as Sala's "excavated cords" tap the independently developed lymphatic spaces around the ccelio-mesenteric artery of the bird.
If this suggestion as to the essentially identical processes of jugular lymph heart development in avian and mammalian embryos should prove true on careful revision of the lymphatic ontogeny of the chick, then the phylogenetic lymph heart record would read as follows:
Fishes : Eudimentary. Amphibia: Fully developed. Urodeles: Multiple (14-20).
AxuREs: Number reduced to two pairs, cephalic and caudal li/mpli hearts. Eeptiles : Caudal heart retained in adult.
Birds: Caudal heart developed ontogenetically, apparently of functional value during the embryonal period. Disappears shortly after adult conditions are established, except in certain forms. Cephalic heart rudimentary, involved in establishment of secondary lymphatico-venous connections. Mammals: Lymph heart formation not carried to point of contractility. Caudal heart rudimentary. Details of its development from venous system not yet established completely. Cephalic heart, as the modified jugular lympli sac, establishes the definite secondary lymphatico-venous connections.
Explanation of Figures
In all figures the following color scheme has been used :
Systemic Veins: White.
Systemic Lymphatics, formed by confluence of perivenous spaces : Yellow.
Veno-lyinphatics, components of the adult lymphatic system derived from embryonal veins, as the avian lymph heart and the mammalian jugniar lymph sac : Blue.
Figs 1-5 inclusive represent schematically the development of the posterior lymph heart and its comiections with the systemic lymphatics in the embryo of the chick, as published by Sala. The figures are reconstructed in schema from Sala's description and from the plates accompanying his paper.
Figs. G-10 inclusive represent in schema the development of the jugular lymph sac and its connections in the embryo of Fells domestica. as determined by Huntington and McClure.
Fig. 1. Early stage in development of the chick's posterior lymph heart. Dilatation of the lateral branches of the first five coccygeal veins, extending into the sui'rounding mesench.vme.
Fig. 2. Confluence of the five dilated venous extensions to form rudiment of the single lymph heart. Scattered muscular fibers in the condensed pericardiac mesenchyme.
Fig. 3. Further development of the lymph heart. Intracardiac septa or partitions resulting from fusion of the five originally sei)arate venous derivatives. Cardiac nuiscular layer completely developed, in direct contact with endocardial endothelial lining.
The Anatomical Eecord.
Fig. 4. Lymph heart and perivenous lymphatic spaces of right side. Differentiation of cardiac wall into a superficial muscular layer and a deep layer, composed of endothelium and a supporting connective tissue stratum. Intracardiac diaphragmata disappear, the lymph heart forming a single cavity, which has lost its original connections with the lateral branches of the first and fifth coccygeal veins, but retains the connections with the three intermediate veins. Beginning formation of one or two cardiac lymphatic vessels, proceeding from the heart to the plexus of independently developed systemic lymphatic vessels surrounding the two hypogastric veins and their median cross-anastomosis.
Fig. 5. Final stage. Lymph heart and systemic lymphatic connections of left side. Lymph hearts communicate by one or two cardiac lymphatic vessels with the general systemic lymphatics, which have formed by confluence of perivenous spaces around the hypogastric veins, their median anastomosis, and their venous tributaries.
CHRONOLOGY OF LYMPHATIC DEVELOPMENT OF CHICK, , AFTER SALA.
1. First outlines of posterior lymph hearts appear middle of 7th day.
2. Muscle fibers appear in cardiac walls second half of 9th day.
3. Connection of lymph heart with first and fifth coccygeal veins interrupted from 11th to 12th day.
4. Independently formed lymphatic spaces appear around hypogastric venous plexus end of 9th day.
5. Communication established between general lymphatic system and hearts end of 10th day.
6. Lymph hearts increase in size from 8th to loth or 16th day. From 16th to 20th day lumen of cavity remains the same, the walls increasing in thickness.
7. Traces of lymph heart formation persist in young chickens up to the 30th or 35th day of free life.
Fig. 6. Embryo of Cat. Early stage in development of the veno-lymphatic sinus, preceding formation of jugular sac.
Composite schematic figure based on plastic reconstruction of the following embryos :
5-6 mm. Both sides (Princeton University Embryological Collection, Series 30).
5-6 mm. Right side (Princeton University Embryological Collection, Series 31).
6.2 mm. Left side (Columbia University Embryological Collection, Series 109).
7 mm. Left side (Princeton University Embryological Collection. Series 2).
7.25 mm. Both sides (Princeton University Embryological Collection, Series 13).
The Anatomical Jiccord. 45
Fig. 7. Second stage. Veno-lyniplintif simis developed in three main divisions, still entirely separated from each other.
Composite scliemalic fi^'urc l)iised on reconstrnctions of the following embryos :
7 mm. Left side. Columbia University Embryological Coll., Series 138.
8.5 mm. Both sides. Columbia University Emliryological Coll., Series 102.
mm. Roth sides. Princeton University EniI)ryological Coll., Series 19.
nun. Left side. Cohuiil)ia University Embryological Coll., Series lOH.
10 mm. Left side. Colunibiii TIniversity Eniliryological Coll., Series 112.
10 nun. Left side. Columbia University T^mliryological Coll., Series 118.
10 mm. Left side. Columbia University Enii»ryol(tgical Coll., Series 114.
Fig. 8. Third stage. Confluence of veno-lymphatic components. Keduction of early multiple connections between the veno-lymphatic sinus and the permanent veins. Evacuation of sac. Appearance of isolated independent perivenous lymphatic spaces, preceding the development of the fully formed systemic lymphatics.
Composite schematic figure based on reconstructions of the following embryos :
10.5 mm. Both sides. Columbia University Embryological Coll., Series 101.
11 mm. Both sides. Columbia T'ni versify Embryological Coll., Series 77.
Fig. 9. Fourth stage. Primary lymphatic condition. Evacuated sac completely detached for a time from the veins. Junction of same with independently formed perivenous systemic lymphatic vessels.
Comi)osite schematic figure based on reconstructions of the following embryos :
10.7 mm. Both sides. Harvard University Embryological Coll., Series 474.*
12 mm. Both sides. Columbia TIniversity Embryological Coll., Series 78.
Fig. 10. Final stage. Secondary or definite lymphatic condition. Fully formed jugular lymph sac of the later embryonic stages and of the adult. Secondary connection of the sac with the venous system and with tlH> goner. il systemic lymphatic vessels. Relative reduction of .iugular sac.
Composite schematic figure based on reconstructions of the following embryos and on dissections of a number of adult animals :
14 mm. Left side. Princeton University Embryological Coll., Seri(<s .^7.
15 mm. Left side. Princeton TIniversity Embryological Coll.. Series l(i.
17 mm. Left side. Princeton University Embryological Coll.. Series 8(;.
18 mm. Both sides. Columbia TTniversity Embryological Coll., Series 88. 25 nun. Both sides. Princeton TIniversity Eniliryological Coll., Series 22.
I owe the opportunity of exniiiinins tills embryo to tlic kindness of Prof. C. S. Minot, of Harvard University.
Cite this page: Hill, M.A. (2021, April 23) Embryology Paper - The genetic interpretation of the development of the mammalian lymphatic system (1908). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_genetic_interpretation_of_the_development_of_the_mammalian_lymphatic_system_(1908)
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