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MEMOIRS 

OF 

THE WISTAR INSTITUTE OF ANATOMY AND BIOLOGY 

No. 1 



THE ANATOMY AND DEVELOPMENT OF 

THE SYSTEMIC LYMPHATIC VESSELS 

IN THE DOMESTIC CAT 



GEO. S. HUNTINGTON 

FROM THB ANATOMICAl. LABORATORY OP COLUMBIA UNIYRRSITT 



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PHILADELPHIA, PA 
1911 

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COMPOSED AND PHINTSD AT THE 

WAVERLY PRESS 

Hy the Williams & Wilkinb Company 

Baltimork, r. S. A. 









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PilS3 

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CONTENTS 

Introduction o 

Part I. The development of the systemic lymphatic vessels in their relation 

to the blood-vascular system U 

Historical review of theories of lymphatic development 10 

Material used in present investigation 16 

Comparison of haemal and lymphatic vascular development 19 

Ontogeny of mammalian systemic lymphatic vessels 24 

Mutual relations of developing systemic lymphatic vessels and embryonic veins 27 

Phylogenetic relations of the abdominal veins and axial lymphatics in 

mammals 33 

Development of systemic lymphatic vessels in the mammal independent of topographical association with embryonal veins 40 

Summary and conclusions of Part 1 53 

Figs. 1 to 28 
Part II. The development of the preazygos and azygos segments of the thoracic ducts 55 

1. The thoracic duct approach of the jugular lymph sacs 60 

Figs 29 to 91. 

2. The preazygos segment 83 

Adult conditions 84 

Figs. 92 to 99. 

.4 . The development of the broncho-me<liastinal trunk 91 

Figs. 100 to 158. 

ti. The development of the preazygos segment of the thoracic duct 107 

Figs. 159 to 169. 

(\ Junction of preazygos segment of thoracic duct and bronchomediastinal trunk with each other and with the thoracic duct 
approach of the jugular lymph sac 113 

Figs. 170 to 187. 

3. Azygos .segment 121 

A. Cleneral analysis of the development of the thoracic duct in the 

azygos region 12,3 

Figs. 188 to 193. 

B. Detailed consideration of the individual stages in the development 

of the azygos segment of the thoracic duct 129 

Junction of azygos and preazygos segments of the thoracic duct 150 

Figs. 194 to 275. 

Summary and conclusions of Part II 153 

3 



43174 



INTRODUCTION 

I have recently published in a preliminary communication,^ a 
r6sum6 of the results obtained in an investigation of manmialian 
lymphatic development and organization extending over the 
past six years, and now, in its main chapters, concluded. The 
paper above quoted was presented, with demonstrations of 
slides, at the 25th session of the Association of American Anatomists held in Boston during Convocation week of 1910, 
and is intended as an attempt to definitely establish what I 
believe to be the genetic principle upon which all systemic 
lymphatic development in the mammalian embryo is based. 
In outline this matter was also presented and demonstrated to 
the Section of Anatomy and Embryology of the XVIth International Medical Congress held at Budapest, August-September, 
1909, and published in the Proceedings of the Congress.^ 

Owing to the character of the problem and its complexity, a 
detailed consideration of the same exceeds the reasonable limits 
of an article suitable for publication in our current anatomical 
periodicals, and the unavoidable number of microphotographic 
illustrations demanded makes publication through the ordinary 
channel still more unadvisable. For these reasons I have arranged, with the cooperation of The Wistar Institute of Anatomy, 
through Director Greenman, to publish the details of my observations on mammalian lymphatic ontogeny in the form of a 
series of monographs, in which the subject can be handled with 

* G. S. Huntington: "The Genetic Principles of the Development of the Systemic Lymphatic Vessels in the Mammalian Embrj'o." Anat, Record., vol. iv, 
no. 11, 1910, pp. 399 to 403, with 32 illustrations. (18 plates.) 

• G. S. Huntington: **Ueber die Entwicklung desLymphatisc hen Systems beim 
Sauger-Embryo." Compte-RendUf xvi. Congres International de Mddecine, 
Section 1, Anatomie, Embryologie, 2. Fascicule, pp. 127-142, Budapest, 1910. 



6 INTRODUCTION 

less restraint than in one of the current publications. I have 
been led to the undertaking largely by my conviction of the value 
of the work which has been done within the last decade in this 
field by American investigators. The development of the lymphatic system is one of the very few broad morphological 
problems as yet incompletely solved, and I believe that the painstaking, able and conscientious work of the relatively large number of interested investigators of the subject in this country wUl 
eventually furnish a satisfactory answer to the question, as a 
national contribution to the advancement of anatomical science. 

I have been obliged to differ, on the basis of my own investigations, from the conclusions reached by most of my American 
colleagues. I hence welcome the opportunity of placing my results 
fully on record, in such a manner that they can be readily examined 
and verified, if correct, or refuted, if found to be erroneous. In 
carrying out this purpose it is of course necessary, in order to 
avoid repetition and economize space, to simply refer to those 
parts of the subject which have been already fully covered in 
the existing, publications, and to include these articles as part 
of the entire record. The main problem then is narrowed down 
to the developmental history of the mammalian systemic 
lymphatic channels, as distinguished from the jugular lymph 
sacs, or other homologous structures of like origin and equivalent 
functional significance, wherever situated. 

The proposed series of publications will include the following 
topics in the order given: 

Part I, The development of the systemic lymphatic vessels in 
their relation to the blood vascular system. 

Part II. The development of the preazygos and azygos segments 
of the thoracic ducts. 

Part III. The development of the visceral lymphatic drainage j 
and especially of the lymphatics of the abdominal cavity; the formation of the receptaculum, and of the postazygos segment of the thoracic ducts, as well as the lymphatic return from the pelvic and caudal 
regions and from the posterior extremity. 



INTRODUCTION 7 

Part IV. The development of the main lymphatic trunks , other 
than the thoracic ducts y draining into the jugular lymph sacs, and 
ctirough them into the venous system, viz., the cervical, jugular and 
supra-scapular lymphatics, and their mediastinal connections, and 
the lymphatic return from the anterior extremity along the subclavian vein. 

Part V. The interpretation of adult normal and variant lymphatic organization on the genetic basis, and the interdependence 
of the adult venous and lymphatic systems. 

The present publication includes Parts I and II of the above 
list. 



PART I 

THE DEVELOPMENT OF THE SYS'^EMIC LYMPHATIC 
VESSELS, IN THEIR RELATION TO THE BLOODVASCULAR SYSTEM 

The question as to the origin of the lymphatic vessels has, 
especially since 1902, occupied the attention of a number of 
American observers. These investigations have followed the 
older work on the same subject of Langer ('68), Budge ('80-'87), 
Gulland C94), Ranvier C95-'97) and Sala (1900), and the results 
have been published chiefly in the American Journal of Anatomy^ 
and in the Anatomical Record.* 

During the progress of these researches a niunber of facts of 
primary importance bearing on the problem of lymphatic development and organization have been discovered. Some of these 
facts have been worked out in detail and are based on sufficiently 
extensive material and acciu'ate observation to carry conviction by their constancy and consistency and to warrant their 
acceptance as definitely established ontogenetic conditions in 
the mammalian embryo. Other observations still lack complete 
confirmation, and in some others the methods employed in their 
determination create a doubt as to their validity, and tend to 
confuse the subject. Finally there are other conditions concerning which there still exists ah honest difference of opinion, and 
which hence require further study and definite determination. 
On the whole, however, the American work of the last six or 
seven years has led to considerable and permanent advance in 

» Vol. i, 1902; vol. iii, 1904; vol. iv, 1904; vol. v, 1905; vol. vi. 1907; vol. ix. 1909; 
vol. X, 1910 
* Vol. ii. 1908: vol, iv. 1910. 

9 



10 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

our knowledge of the genesis of the mammalian lymphatic 
system. 

The results so far obtained, and the views based thereon, may, 
with inclusion of the older work on the subject of vertebrate 
lymphatic development in general, be briefly summed up as 
follows in the form of short theoretic statements: 

I. The lymphatic system is developed independently of the 
blood- vascular system. It is formed by the confluence of independently developed mesenchymal spaces, and, in case of the 
avian thoracic duct, by canalization of preformed solid strands 
of differentiated mesenchyme.*'®'^ 

The works of Brachet and the combined researches of Brachet 
and Swaen,*in their relation to the interpretation of lymphatic 
development, also support the independent origin of the lymphatic system from the mesenchyme. 

The interesting observations of Marcus on the development and 
organization of the lymphatic system in Hypogeophis* place the 
conclusions of this investigator in regard to the genesis of lymphatic structures in this general division, with the addition of the 
conception of the coelomata as primary lymphatic spaces (vide 
infra, pp. 25 and 26), and the phylogenetic derivation of the 
peripheral lymphatic system from the same. 

•Budge: "Ueber ein Canalsystem im Mesoderm von Huhnerembryonen." 
Arch, fur Anal, und Phys., Anat. Abth., 1880, .s. 320. "Untereuchungen uber 
die Entwicklung des Lymphsystems beim Htihnerembrj'o." Arch. f. Anat. u. 
Phytt., Anat. Abth., 1887, s. 59. 

• L. Sala: "Sullo sviluppo dei cuori linfatiei e dei dotti toracici nelT onibryone 
di polio." Ricerche fatta nel Laboratorio di Anatomia Normale della R. Univ. 
di Roma, vol. vii, p. 263-269, April, 1900. 

'^G. Lovoll GuUand: "Tlic Dovelopment of Lyniphutic Glands", Jour. Path, 
and Bad., vol. ii, 1894, pp. 447-485. 

 A. Brachet, "Recherches sur le d^velopp. du coeur, des premiers vaisseaux 
ct du sang chez les amphibiens urod^les," Arch, d^anat. microscopique, ii, 1898. 
''Recherches sur I'origine de I'appareil vasculaire sanguin rhez les amphibiens," 
Arch, de Biologic, xix, 1903. 

A. Swaon et A. Brachet, ''ftlude sur les premiers phases du d^velopp. clcs 
organs derives du m^^soblast chez les poissons t^^leostiens," Arch, de Biologic, 
xvi, 1899-1900. 

• H. Marcus, "Bcitriige zur Kcnntnis der Gymnopliionen; II. I'eber intersegmentale Lymphherzen, nebst Bemerkungen iiber das Lymphsystem.'' Morphol. 
Jahrhuch. Bd. xxxviii. Heft 4, 1908. 



RELATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 11 

II. The lymphatic vessels are du-ectly derived from the 
venous system, certain embryonic venous channels being transferred in toto to the lymphatic system.*®' "'^2, is 

III. All systemic lymphatics are formed by union of multiple 
direct derivatives from the embryonic veins," or only the thoracic 
ducts are so developed, while the other sj'^stemic lymphatic vessels arise independently.*^ 

IV. The mammalian lymphatic system as a whole is developed 
by blind ducts which ''bud off'' from the embryonic veins of the 
cervical, and later from those of the inguinal region, widen out 
to form sacs, from which lymphatics grow to the skin and ''cover 
its surface, while at the same time a growth of ducts occurs along 
the dorsal line following the aorta to make a thoracic duct from 
which lymphatics grow to the various organs.'' The theory underlying this conception of lymphatic development assumes the 
primary formation of a number of sacs, derived from the veins, 
and lined by embryonic venous endothelium, from which, as the 

'" C. Langer: ''Ueberdas LjrmphgefiisssystemsdesFrosches." Sitzb. d. Akad. 
d. Wissenschj Bd. Iviii.. I. Abth., 1868. 

" L. Ranvier: Comptes Rendues, 1895, 1896. "Morphologie et developpement 
des vaissaux lymphatiques rhcz les mammifdrcs." Archives d^Anatomie Microscopique, Tome I, 1897. 

** Giuseppe Favaro, ''Richerche intorno alia morfologia ed alio sviluppo dei 
vasi, seni e cuori caudal i nei Ciclostoini e nei Pesci," Atti del Realilnslituto Veneto 
di Scienze, latere et Arti., anno accad. 1905-1906, Toino Ixv, Parte seconda. 
Appendice alia Dispensa X. ''Note fisiologiche intorno al cuore caudale dei 
Murenoidi (Tipo Anguilla vulgaris, Turt.)," Archiv. di Fisiologia, vol. ii, Fasc. 
V, Luglio, 1905. ** II cuori ed i seni caudali dei Teleostei," Anat. Am., xxvii. Band, 
no. 14 und 15, 1905. 

" W. F. Allen, "The Distribution of the Lymphatics in the Head and in the 
Dorsal, Pectoral and Ventral Fins of Scorpaenichthys mamoratus," Proc. Washington Acad, of Sciences f vol. viii, pp. 41-90, May 18 1906. "The Distribution of 
the Subcutaneus Vessels in the Head region of the Ganoids, Polyodon and Lepidosteus,*' ibid.f vol. ix, pp. 79-158. July 1907. "The blood-vascular system of 
the Loricati, the mail-checked fishes," ibid., vol. vii, 1905. 

"Distribution of the subcutaneous vessels in the tail region of l^episosteus," .4m. Jour. Anat. vol. viii, 190S. 

^* V. T. I^wis: "The Development of the Lymphatic System in Rabbits.'* 
Am. Journ. of Anat., vol. v, 1905, pp. 95-111. 

»• C. F. W. McClure: "The Development of the Thoracic and Right Lymphatic 
Ducts in the Domestic Cat." .47ia/. Anz., xxxii. Band, No. 21 and 22, 1908, p. 
534. 



12 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

starting points, the lymph channels of the entire body devolop 
by a process of continuous and uninterrupted centrifugal "sprouting" toward the periphery. "»"»"»^'»*® 

V. The systemic lymphatics are formed by confluence of 
perivenous mesodermal spaces, developed, as separate anlages, 
outside the intima of the early venous channels, but not communicating with the same except at definite points of lymphaticovenous connection which are secondarily formed.*^ 

This view pronounces for the ontogenesis of endothelial cells, 
lining the separate mesodermal spaces, independently of the 
haemal vascular endothelium. The spaces ' forming the first 
anlages of the systemic Ijntnphatic vessels are in no sense derived 
from the embryonic veins, although closely associated with them 
topographicaUy. 

At the time of the publication of the paper embodying these 
views, McClure and I were not aware of the important r61e 
played by the jugular lymph sacs, as affording the portals of 
entry of the entire systemic lymphatic circulation into the 
venous system. This relation was only subsequently ascertained 

" F. R. Sabin: "On the Origin of the Lymphatic System from the Veins, and 
the Development of the Lymph Hearts and Thoracic Duct in the Pig/' Am. Jour. 
AnaL, vol. i, 1902, pp. 367-389. "On the Development of the Superficial Lymphatics in the Skin of the Pig/' Am. Jour, AnaL, vol. iii, 1904, pp. 183-195. "The 
Development of the Lymphatic Nodes in the Pig and the Relation to the Lymph 
Hearts," Am. Jour. Anat., vol. iv, 1905, p. 355-389. "Further Evidence on the 
Origin of the Lymphatic Endothelium from the Endothelium of the Blood Vascular System," Aruit. Record., vol. ii, 1908, pp. 4&-54. "The Lymphatic System 
in Human Embryos, with a Consideration of the Morphology of the System," 
Am. Jour. Anat., vol. ix, 1909, pp. 43-90. 

" W. J. MacCallum: "Die Beziehung der Lymphgefasse zum Bindegewebe." 
Arch. f. Anat. und Phys., Anat. Abth., 1902. 

" G. Heuer: "The Development of the Lymphatics in the Small Intestine of the 
Pig." Am. Jour. Anat., vol. ix, no. 1, 1909. 

" W. A. Baetjer : ' The Origin of the Mesenteric Lymph Sac in the Pig." A nat. 
Record, vol. ii, 1908. 

*® H. Hoyer, ''Untersuchungen uber das Lymphgefasssystem der Froschlarven. 
I. Theil." Extrait du Bulletin de V Academic des Sciences de Cracovie, CI iss2 des 
Sciences mathemaliques et naturelles. Juillet, 1905. II. Theil, ibid., Mai, IQOvH. 

" G. S. Huntington and C. F. W. McClure: "The Development of the Main 
Lymph Channels of the Cat in their Relation to the Venous System." Am. J our. 
Anat., vol. vi, 1907. Abstr. Anat. Rec., vol. i, pp. 36-41. 



RELATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 13 

in the course of a detailed joint investigation of the development 
of these organs. We consequently failed to correctly recognize 
the origin of the adult lymphatico-venous junctions, and regarded 
them as direct secondary connections of the systemic lymphatics 
with the veins. The paper quoted, however, describes the 
genesis of the lymphatic vessels in their relation to the venous 
system correctly. 

VI. In 1907 I published,^ based on McClure's and my own 
joint investigations, a genetic interpretation of the development 
of the mammalian Ijntnphatic system as a whole, in which I defined 
the same as the product of the union of two genetically different 
and very unequal portions: 

1. The entire extensive system of the lymphatic vessels 
proper of the adult animal, including the thoracic and right 
lymphatic ducts and their tributaries, is formed by the confluence 
of extra-venous intercellular mesodermal spaces, in the sense 
above defined (V). 

These spaces are lined by a lymphatic vascular endothelium 
which is not derived from the haemal vascular endothelium, but 
develops independently of the same. The lymphatic channels, 
which result from the confluence of these spaces, follow in large 
part the embryonic veins closely, but they are neither derived 
from them, nor do they communicate with them, except at 
definite points, at which the rudimentary mammalian type of 
lymphatico-venous heart is developed. 

2. A definite structure, the Jugular Lymph Sac, develops 
in the prevalent and typical mammalian lymphatic organization, 
directly from a perivenous capillary reticulum of the early preand postcardinal veins, adjacent to and including their point of 
confluence to form the duct of Cuvier. This jugular lymph sac, 
or rudimentary homologue of one of the lymph hearts of lower 
vertebratcKS, arising directly from the veins, subsequently separates for a short period entirely from the same, and finally makes 
two sets of permanent connections: 

^ G. S. Huntington: ''The Genetic Interpretation of the Development of the 
Mammalian Lymphatic System.'' Anat. Record, vol. ii, 1908, pp. 19-45. 



14 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

(a) With the above defined independently formed systemic 
lymphatic channels of the entire body. 

(6) Secondary connections with the venous system, re-entering 
the same at one or more typical and constant points, and thus 
forming the link which finally unites the venous and the lymphatic 
systems, developed independently of each other. 

The above are, briefly summarized, the views of lymphatic 
development based on recent observations. 

It will be seen, as previously stated, that opinions still differ 
as to the origin of the first lymphatic anlages and their subsequent method of growth, and as to the genetic derivation of the 
lymphatic vascular endothelium. 

The following two main questions are therefore still to be 
definitely answered: 

(1) Is the adult mammalian lymphatic system the result of 
continuous and uninterrupted growth from one or more central 
points toward the periphery, or is it genetically a channel system, 
developed on the same lines as the primary blood vascular system, by the confluence of a number of originally separate and 
independent anlages? 

(2) Is the lymphatic vascular endothelium of the mammal 
derived from pre-existing haemal vascular endothelium, or is it 
the result of independent modification of mesodermal cells? 

It now remains to answer definitely these questions, and, on 
the evidence of sufficiently extensive material and careful observations, to clear the field of theoretical considerations, and to 
establish, as far as possible, by sound methods and on a broad 
basis, the genesis of the mammalian lymphatic system as a whole. 
It is evident that an interpretation, which assumes to fulfill these 
conditions, must be capable of accurately standing the test of 
both ontogenetic and phylogenetic consistency. 

Believing, as I do, and have, since my first expression of opinion 
on the subject, that the principles embodied in the genetic interpretation of mammalian lymphatic development above outlined 
(VI) are correct, I have undertaken to establish their truth by a 
detailed critical study of the lymphatic system, both in the 
adult and in the embryo, in one mammalian form, the Domestic 



RELATION OF LYMPHATIC TO BLOOD- VASCULAR SYSTEM 15 

Cat, which animal, by reason of its clear-cut type of venous 
development,*' and the great range of its adult venous variation,"* *^ seemed to me to offer the best opportunity of viewing 
the problem of mammalian lymphatic development both from 
the standpoint of its normal course in a representative form, and 
with reference to the variant conditions imposed upon it by 
correlated variants in the organization of the main systemic veins. 

I have been further influenced in my selection of the cat 
for special and detailed study by the fact that in my experience 
the embryos of this carnivore offer uniformly histological pictures 
of lymphatic ontogenesis which are far more definite, clean-cut 
and conclusive than those obtained in ungulate, rodent or marsupial embryos. I believe that the cat is the only known available 
mammal in which the facts of systemic lymphatic development, 
as set forth in the following pages, could have been definitely 
ascertained. Guided by the clue thus furnished, it is not difficult to determine, by comparison, the existence of absolutely 
corresponding developmental conditions in the embryos of the 
pig, rat, rabbit, and opposum. But in none of these forms are 
the typical genetic stages as clearly marked and the tissues as 
definitely differentiated as in the cat. 

The investigation of mammalian lymphatic development 
divides itself naturally, in accordance with the postulates of the 
genetic theory above advanced (VI), into three separate and 
distinct main parts: 

(1) The development and adult anatomy of the jugular 
lymph sacs. 

(2) The development and adult anatomy of the general 
systemic lymphatic vessels. 

" Ct. S. Huntington and V. V. \V. McClure: "The Development of the Posteuva 
and Tributaries in the Domestic Cat." Am. Jour. Annt., vol. vi, 1907, Abstr. 
Anat. Record, vol. i. 

•* Wm. Darrach: "Variations of the Postcava and its Tributaries in 605 Examples of the Domestic Cat." Am. Jour. Aunt., vol. vi, no. 3, 1907, Abstr. Anat. 
Record, vol. i, p. 30. 

»G. S. Huntington and C. F. \V. McClure "The Interpretation of Variations 
of the Postcava and Tributaries in the Domestic C/at, bjised on their Development." -4m. Jour. Annt., vol. vi. 1907. Abstr. Anat. Record, vol. i, p. .33. 



16 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

(3) The mode of union with each other of the two components 
just enumerated, and the resulting establishment of a continuous 
centripetal lymphatic vascular system, with definite and constant 
terminals in the venous trunks. The first part of this work has 
been completed in conjunction with Prof. C. F. W. McClure 
of Princeton University. The results of our joint investigation 
on the development and structure of the jugular lymph sacs 
of the Cat have been published in a preliminary account.*® The 
details, with critical analysis of a large series of embryos, and 
illustrations of the reconstructions of all the important stages, 
are given in an extensive paper recently published." 

In these publications McClure and I have definitely demonstrated the fact that in the embryo of the cat the jugular lymph 
sacs develop as a small, but vitally important, part of the entire 
lymphatic system, directly from the pre- and postcardmal veins 
and their tributary plexuses, near to and including their Cuvierian junction. 

The genesis of the jugular lymph sacs and their share in the 
adult organization having been thus definitely established in 
detail, I intend to follow independently the second postulate 
of the theory of the composite character of the adult mammalian 
lymphatic system above outlined (VI), and to show that the 
jugular lymph sacs, of direct venous origin, constitute the links 
uniting the hsemal vascular system and the general systeri of 
the lymphatic vessels, the latter developed independently of the 
veins, by the confluence of intercellular mesenchjntnal spaces 
surrounding, for the most part, the embryonic venous channels, 
but in no sense derived from the same. 

MATERIA 

For the reasons stated above I have chiefly used the embryos 
of the domestic cat. Of these I have examined the following 
107 individual embryos in complete serial sections: 

* G. S. Huntington and C. F. W. McClure: ''The Anatomy and Development 
of the Jugular Lymph Sacs in the Domestic Cat." Anal. Recordy vol. ii, 1908, 
pp. 1-18. 

" American Jour. ofAnat., vol. x, no. 2, April, 1910, pp. 177 to 311 with 67 figures. 



RELATION OP LYMPHATIC TO BLOOD-VASCULAR SYSTEM 



17 



tBRIKS NO. 

188 11 Somites 

86 13 Somites 

CKOWN RUMP 
MEASURE 

(TAKEN 
ArTEK 

fixation) 
mm, 

82 4.5 

93 4.5 

226 5.18 

110 5.6 

138 5.6 

103 5.7 

84 6 

85 6 

115 6 

116 6 

117.. 6 

128 6 

187 6 

109 6.2 

129 6.5 

130 6.5 

131 6.5 

186 6.5 

105 6.8 

135 7 

137 7 

108 7.2 

119 7.2 

121 7.2 

S9 8 

102 8 

75A 8.5 

106 9 

136 9.2 

132 9.5 

133 9.5 

230 9.5 

79 10 

101 10 

111 10 

112 10 

113 10 

114 10 

. 140 10 

237 10 

81 10.3 



CROWN RUMP 
MEASURE 

(taken 

AFTER 
FIXATION) 

SERIES NO. mm. 

• 118 10.5 

120 10.5 

77 11 

98 11 

213 11 

256 11.5 

78 12 

97 12 

100 12 

217 12 

92 13 

107 13 

76 13.5 

189 13.5 

223 13.5 

127 14 

210 14 

211 14 

212 14 

214 14 

75 15 

91 15 

216 15 

218 15 

219 15 

243 15 

244 15 

245 15 

246 15 

141 15.6 

143 15.5 

215 15.5 

247 15.5 

95 16 

96 16 

222 16 

224 16 

230 16 

248 16 

240 16.5 

94 17 

142 17 

198 17 

258 17 



18 



DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 



CROWK RUMP 
MBA8URR 

(takbn 

AFTER 

fixation) 
BBRIB8 NO. mm. 

87 18 • 

88 18 

199 18.6 

249 18.5 

250 18.5 

254 18.5 

80 19 

197 19 

252 19 

253 19 



CBOWNBCMP 
MEASURE 

(taken 

AFTER 

fixation) 
SBRIE8 NO. mm. 

83 20 

255 20 

241 20 

242 21 

147 25 

168 34 

144 31.5 

90 35 

104 51 



These embryos are contained in the Embryological Collection 
of Columbia University. The majority of the preparations were 
fixed in Zenker's fluid and stained differentially on the slide 
with Haemotoxylon (Delafield) and Orange-G. 

I have also had, through the courtesy of Professor McClure, 
the opportunity of carefully examining three very interesting 
cat embryos of the Princeton Collection, series 34 and 37, each 
of 14 mm. crown-rump measure, and series53, al5mm. embryo. 

A series of 180 adult animals with successful injection of the 
main systemic lymphatics served as control for the embryological determinations, and for the comparison of normal and variant 
adult conditions of the venous and lymphatic systems with the 
corresponding ontogenetic stages. 



The results of my observations on the development of the 
mammalian systemic lymphatic vessels, as distinguished from 
the jugular lymph sacs, studied jointly with McClure, may be 
briefly summed up as follows: 

The systemic lymphatic vessels of the entire body are formed 
through confluence of numerous originally separate intercellular 
mesodermal spaces, which develop bx great part in close apposition to the walls of the embryonic venous channels, and in exactly 
the same way as the primary anlages of the hsemal vascular 
system, but independent of the latter. The endothelium lining 
these first anlages of the lymphatic vascular channels is from the 



RELATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 19 

beginning independent of the hsemal endothelium, and develops 
with the first appearance of the lymphatic spaces, from the 
indifferent mesodermal cells lining these spaces. In my opinion 
the lymphatic and haemal vascular endothelium have the same genetic derivation from the modified mesodermal cell lining the tissue 
spaces. The primary stage of endothelial differentiation is the 
same, whether the resulting channel system is to be assigned to 
the hsemal or the lymphatic division of the vascular system. 
We have therefore two generations of the embryonic vascular 
endothelial cell, a hsemal and a lymphatic. Both develop in 
the same way and as the result of identical genetic factors from 
the indifferent mesodermal cell. Both are from the very beginning of the process independent of each other in the mammalian 
embryo. 

I desire again to emphatically aver my conviction that all the 
systemic lymphatic vessels of the mammalian embryo, including the thoracic ducts and their tributaries, are neither in their 
genesis continuous ''outgrowths'' or ''buds'' from sacs of venous 
origin, wherever situated, nor derived from multiple outgrowths 
from the embryonic veins, such outgrowths subsequently separating from the veins and fusing into continuous lymphatic channels. 
They are, in my opinion, on the contrary, from their very first 
inception, independent of the haemal vascular system, and their 
endothelial lining is not derived from the blood vascular endothelium. They develop as independent intercellular mesodermal 
spaces, which become confluent with each other to form larger 
and larger communicating channels. These finally attain their 
entrance into the venous system through the intervention of 
the jugular lymph sacs, in the manner outlined in the publications above quo ted. 22 '26, 27 

Before taking up the details of the development of the first 
lymphatic anlages in the mammalian embryo, it seems advisable 
to refer briefly to a r^sum^ of known facts in regard to the earliest 
formative stages of the blood vascular system, in order to facilitate the comparison between haemal and lymphatic development. 

Phylogenetically, the earliest form of a closed circulatory 
system in multicellular organisms consists of intercellular canals 



20 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

conveying a clear plasmatic fluid without cellular contents. 
The same picture is presented in the earliest stages of hsemal 
development in vertebrates. Thoma's^® investigations of the 
histogenesis of the blood vascular system in chick embryos have 
furnished us with a very clear picture of the process. 

The first histogenetic inception of the vertebrate hsemal 
vascular system is marked by the condensation of the mesoderm 
into cellular strands. Between the cells of these praevascular 
strands multiple oval or round spaces develop, which enlarge, 
elongate and become confluent, forming a network of inter-communicating channels, the hcBmal capillary anlages. These channels contain a clear colourless fluid, with no, or only very scattered, cellular elements. This fluid, obtained by secretion from 
the free surfaces of the cells limiting the spaces, is evidently 
under a certain definite pressure, which exerts an influence on 
the form of the cells lining the channels. These limiting cells 
lose their earlier isodiametric, more or less regular cuboidal form, 
and appear flattened, and on optical section spindle-shaped. 
They have begun to assume the endothelial character. Hence 
from its earliest inception the endothelial lining of vascular 
channels appears as an enviroiunental adaptation of the mesodermal cell. One surface of a cuboidal cell is freed from contact with adjacent cells by the development of an intercellular 
cleft, and this free surface is subjected to the pressure of the 
fluid contained in the earliest capillary anlages, modified by the 
tension pressure of the organism as a whole. This mechanical 
adaptation to the altered cellular milieu results in the formation 
of endothelium, and the process is identical in all portions of 
the mesoderm, independent of the question as to whether the 
resulting endothelial lined space shall subsequently be incorporated in a haemal or a lymphatic system of vascular channels, 
or shall remain as a closed non-vascular mesodermal space. 

It seems to me futile to try to speculate on an ontogenetic 
stage in which endothelium acquires a "specific'' character. It 

^■R. Thoma: ''Untersuchungen uberdie Histogenese und Histomechanik des 
Blutgefasssystems/' Stuttgart, 1893. 



RELATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 21 

develops de novo in the adult under appropriate normal conditions. 

Furthermore, this endothelial characterization of modified 
mesodermal cells is from the beginning a multiple process, starting independently at innumerable separate and discrete points 
of the vascular area, and becoming only subsequently continuous 
by confluence of the individual separate anlages. This fact is 
of importance in drawing general conclusions as to the later 
extension of vascular endothelium, whether haemal or lymphatic. 

Up to this point the histogenetic and physical characters of 
all developing vascular structures are identical. The picture 
just described applies equally to the earliest definite anlages of 
the haemal capillary system, and, as I shall show, to the first 
appearance of the earliest lymphatic structures of the body. 
In the case of the definite blood-vascular channels of the vertebrate embryo, however, a further developmental change occurs, 
namely, the addition of free, specially modified, mesodermal 
cells, as the red blood cells, to the clear plasma circulating in the 
channel-system of the earliest capillary anlages in response to 
the first pulsations of the heart. 

The first blood vessels of the area pellucida appear, at least 
in part, to develop independentlyof the so-called ''Blood islands.'' 
These latter, originally, form broad cellular strands composed of 
closely packed uncolored cells, which are only distinguished from 
the solid strands of the earliest vascular anlages of the area pellucida by greater size and massiveness. After the vascular cellstrands of the area pellucida have developed in their interior the 
intercellular closed oval or round spaces of the first capillary anlages, 
similar spaces also appear in the more massive cell strands of the 
peripheral portion of the area vasculosa. In the subsequent 
confluence of these discretely developed spaces to form the early 
capillary reticulum, the blood islands become more and more 
surrounded by the forming channels and are thus separated from 
the adjacent tissues. New endothelial-lined spaces continue to 
develop on the surface of the blood-islands, enlarge and join the 
system of connected channels. The cells forming the walls of 
these primitive capillaries become, as above stated, transformed 



22 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

into the typical flattened endothelial cells of the vascular intima. 
Excepted from this endothelial transformation are only those 
cells of the vascular walls which differentiate as young blood cells. 
Thus eventually the confluence of the originally individual and 
separate spaces produces a continuous and connected channel 
system, lined by endothelium, which nearly encircles the blood 
islands. The latter are therefore now in large part included within 
the lumen of the capillaries, with whose walls they are from place 
to place continuous. It only requires a further and complete 
solution of this continuity, and the accompanying freeing of the 
blood cells, to add the latter to the plasma circulating in the 
preformed channels. In the chick, according to Thoma's observations, the resolution of the blood islands into separate blood 
cells occurs between the 45th and 55th hour of incubation, while 
the acquisition of haemoglobin by the cells occurs between the 
40th and 45th hour. With this occurrence the development of 
the primary blood-vascular channels has reached its definite 
accomplishment. 

The general picture presented by the earliest development of 
the blood-vascular system may therefore be summarized as follows: 

(1) Differentiation of certain mesodermal areas and lines by 
the multiplication of mesodermal cells to form cell-strands of 
varying density and size (vascular strands). 

This appears to be a common antecedent condition not only 
of all vascular mesodermal structures, but also of other mesodermal derivatives eventually destined to obtain a lumen and 
enter into the formation of canals, as the Wolffian tubules and 
the cell-strands of the gonad. 

It possibly explains the conditions described, for example, by 
Sala in the development of the avian thoracic duct, is seen 
in the developing aortae of early chick embryos, and is especially 
significant in the pictures furnished by Sabotta of the development of the aortae in fishes. 

(2) Development in the interior of these cellular strands of 
intercellular spaces in large numbers. 

(3) Bio-mechanical modification of cells lining these spaces 
to produce typical flattened vascular endothelium. 



RSLATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 23 

(4) Confluence of these endothelial-lined spaces to form 
larger and larger vascular areas of intercommunicating channels, 
containing a clear plasmatic fluid, which circulates in the channels in response to the establishment of cardiac pulsation. 

(5) Addition to the plasmatic contents of these channels, 
coincident with their further growth and extension into a continuous circulatory system, of cellular elements, derived from 
the mesoderm and specially modified to acquire haemoglobin 
and function as red blood cells. These cells, by solution of 
tissue continuity, are liberated from the blood islands which are 
first surrounded by the confluent spaces of the capillary anlages. 

(6) Subsequent differentiation of the adventitia, with specialization of districts by cardiac concentration, amalgamation of 
the plexus into larger arterial and venous channels, definition 
of permanent capillary areas, valve and septal formation, etc. 

The striking features of this ontogenetic history of the blood 
vascular system are: 

1. The relatively late addition to the preformed non-cellular 
circulation of free cell elements, which, as the red blood cells, 
stamp, from the period of their liberation and inclusion in the 
circulating plasma, the resulting vascular system as fujemal, 

2. The common origin from mesoderm of both characteristic 
components of the haemal system, viz., the vascular endothelium 
and the red blood cell. Both the vascular intima and the free 
cell contents of the channels lined by this intima appear as highly 
modified derivatives of the same mesodermal cellular ancestors, 
which constitute the cell-strands of the earliest period of vascular 
development. In their first inception the systemic lymphatic 
vessels of the mammalian embryo, as distinguished from the 
jugular lymph sacs of venous origin, repeat in every detail the 
primary stages of the developing haemal capillaries, prior to the 
inclusion within the lumen of the latter, of the cellular contents 
of the blood islands. They can be identified as distinct structures as soon as the blood channels proper have differentiated. 
Before that period direct observation cannot determine, in case 
of individual mesenchymal spaces, whether they are eventually 
to become part of the lymphatic or of the blood vascular system. 



24 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

It is therefore quite possible that in the mammalian embryo both 
sets of intercellular mesodermal spaces develop side by side and 
simultaneously, although prior to the setting free of the hsBmoglobin cells and their appearance within the lumen of the haemal 
capillaries, there is no absolute criterion which would serve to 
distinguish intercellular spaces as belonging definitely to either 
the haemal or the lymphatic division of the general vascular 
anlage. 

It hence appears to me futile to base serious conclusions in 
regard to the genesis of vascular structure on observations made 
on the vessels seen in the transparent tails of living anure amphibia. Phylogenetically, from the urodele standpoint, such 
larvae are adult organisms. We all know that, once established, 
all divisions of the vascular organization are, under the stimulus 
of normal or abnormal growth, capable of further increase and 
extension. The observations above referred to may offer, if 
correctly interpreted, interesting side lights on the method of 
vascular growth, but they cannot, in any valid sense, bear on 
the problem of vascular genesis, either haemal or lymphatic. 

But in mammalian embryos of the proper stages, and specifically in embryos of the Cat between 10 and 12 mm., the first 
systemic lymphatic anlages are clearly differentiated in the circumscribed areas of their first appearance, coincident with the 
definition of the early intra-embryonic blood channels. 

Thus in the omphalo-mesenteric district, and cephalad and 
caudad of this point, on each side of the aorta, isolated 
intercellular mesenchymal spaces appear at this period, closely 
applied to the walls of the neighboring venous plexuses of the 
postcardinal and mesonephroic veins, but not connected with 
the same. These intercellular clefts enlarge rapidly to form 
numerous oval or round spaces, closely interwoven with the 
venous network and later with the sympathetic anlages. The 
cells limiting these early lymphatic anlages become, with the 
further extension of the spaces which they line, flattened and 
assume typical endothelial characters. 

Fig. 1 shows a transverse section of a 10 mm. cat embryo 
(series 111, slide viii, section 4) magnified 175 diameters, cephalad 



RELATION OP LYMPHATIC TO BLOOD-VASCULAR SYSTEM 26 

of the mesonephros and the subcardinal cross anastomosis, and 
gives a topographical view of. the region in which the first mesodermal intercellular lymphatic tissue spaces {77) appear, in the interval between aorta {73) , postcardinal vein {68) and coelom {78) . 

Fig. 2 is the same section of this embryo, magnified 300 diameters, and shows the area to the left of the aorta. Between 
this vessel {73) and the well defined left postcardinal vein {68) 
dorsad, and the coelom cavity {78) ventrad, appear a number 
of clear mesenchymal spaces {77) which do not communicate with 
the adjacent venous channels. Some of these spaces extend 
from the coelom angle dorsad along the lateral aspect of the 
postcardinal. They are the first distinctly recognizable anlages 
of the lymphatic system, and they develop, from their first 
inception, as independent mesenchymal spaces, closely related 
to the adjacent haemal channels, but genetically independent 
of the latter. 

Fig. 3 shows the same field in a magnification of 600 diameters. 
The spaces are clearly ciit, separate and distinct, and the limiting cells are beginning to assume endothelial character. 

The relation between the haemal channels and the developing adjacent lymphatic spaces can be clearly traced in successive sections of this same embryo proceeding caudad. 

Figs. 4, 5, 6, and 7 show, respectively, sections 7, 8, 9 and 10 
of slide viii of series 111, magnified 300 diameters. 

In all of these sections the uniformity, and the distinct structural character of the primary lymphatic tissue-spaces is clearly 
visible in the same situation and in identical relation to surrounding structures. 

For comparison with the preceding series the same region is 
shown in another 10 mm. embryo (series 120, slide ix, sections 
25 and 26) in two successive sections, magnified 300 diameters, 
in figs. 8 and 9. 

In these sections the same independent mesodermal spaces 
{77) are seen in their typical relation to aorta {73) , post-cardinal vein {68) and coelom cleft {78). 

The interesting question of the relationship between these 
early mesenchymal spaces and the coelom cavity can only be 



26 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

considered superficially at this time. Yet, in some regions, 
very suggestive pictures are obtained. Thus in section 4 of 
slide viii of series 111 (figs. 1, 2 and 3) the distinct appearance 
of a communication between the coelom cavity proper {78) and 
the early mesenchymal spaces {77) above described is given by a 
clearly limited and well defined funnel-shaped stoma, occuping 
the dorsal extremity of the coelomic cleft {79 in fig. 2), and 
apparently opening directly into the spaces of the early lymphatic plexus. The remaining sections of this series figured 
(figs. 4 to 7) confirm this impression. 

The conditions here described for early embryos of the cat 
strongly support the views expressed by Marcus' in his studies 
on the lymphatic development of Hypogeophis. The microphotographs here given should be compared with his description on 
pp. 599-601 of the paper quoted, with his text fig. 6, and with his 
figs. 5 and 6 of plate xvi. 

The early mesodermal spaces here described and figured are 
lymphatic in character and form part of the extensive temporary 
network of lymphatic channels which appears for a time during 
mammalian ontogenesis and which bears a close resemblance to 
the corresponding lymphatic organization in amphibia and 
reptiles. The peri-aortic lymphatic sinuses and the exaggerated 
subcutaneous lymph channels of the earlier mammalian stages are 
portions of this evanescent and reminiscent system, which subsequently in large part retrogrades, and either disappears altogether 
or is extremely modified to meet the definite permanent conditions of mammalian lymphatic organization. Thus the early 
periaortic spaces become much reduced in course of further development. They then become associated, in a way presently to 
be described in detail, with elements of the axial venous plexuses 
of the mammalian embryo and form the anlages of the main 
segments of the thoracic ducts. This ontogenetic temporary 
recall of antecedent phylogenetic types of vascular development 
appears to be chiefly centered, in the mammalian embryo, in 
the region around the omphalo-mesenteric artery, where, in the 
adult, the definite and permanent lymphatic trunks closely 
resemble in their arrangement the peri-omphalo-mesenteric 
annular veins of certain reptilian embryos. 



RELATION OF LYMPHATIC TO BLOOD- VASCULAR SYSTEM 27 

In the succeeding stages the mesodermal lymphatic anlages 
assume, in large part, the very definite relation to certain embryonic venous channels, which led McClure and myself to describe 
them in 1906 in our preliminary account above quoted,^^ as 
''extraintimaP' or ^'perivenous'' structures. 

This relationship is of two kinds: 

A. Total replacement of temporary embryonic veins by extraintimal lymphatic channels. 

In the earlier embryonic stages the areas of the future definite 
venous channels are largely occupied by an antecedent venous 
or capillary network, out of which, along definite hydrostatic 
lines, the subsequent veins develop by confluence of the plexus elements occupying these lines. ^^ Parts of the early capillary reticulum, not thus included in the path of the definitely organized 
venous trunks, remain, after the latter have become established, 
as a perivenous plexus. Some of the elements of this secondarily 
established plexus develop into permanent tributaries of the 
main veins. Others undergo a process of separation from the 
permanent functional channels and degenerate. In many cases 
their blood-cell contents break down and are eliminated, w^hile 
their endothelial lining appears to revert to the indifferent type 
of the embryonic mesodermal cell. 

Thus in embryos between 13.5 and 16 nmi. many striking 
instances of this reversion are to be observed. The former 
vascular channel appears as a collection of clearly differentiated 
and very highly stained mesodermal cells. 

Figs. 47, 50, 61, in Part II, show these mesodermal vascular 
derivatives very clearly. They form the dark masses seen in 
the field dorsal and dorsolateral to the oesophagus and in the 
peritracheal region. 

In many regions of the mammalian embryo, however, these 
detached and retrograding venous elements do not attain this 
condition, but in an earlier stage, constitute lines around which the 
most active primarj'^ lymphatic organization of the mammalian 

*• H. V. W. Schulte and Fred. Tilney: "Note on the Organization of the Venoufi 
Return, with Especial Reference to the niac Veins." Anal. Record^ vol. iii, no. 
11, 1909. 



28 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

embryo centers. The intercellular mesodermal clefts above 
described develop especially along and around these decadent 
venules and finally envelop them. As the result of this process the 
lymphatic anlages appear in certain mammalian ontogenetic 
stages, in large part, as distinct spaces enclosing the remnant of 
the embryonic vein. The latter may still, for a time, contain a 
few degenerating red blood cells, but these soon disappear, and 
then the entire anlage is formed by a collapsed and empty endothelial tube, the abandoned chaniLel of the earlier vein, surrounded by a second endothelial tube, formed by the confluence 
of the independently developed extraintimal or perivenous mesodermal spaces. As these spaces enlarge and join each other their 
lumen increases, and the limiting cells become flattened and 
assume typical endothelial characters. The height of this phase 
of lymphatic development is reached in embryos of the cat in the 
14 mm. stage, and numerous demonstrations of the appearance of 
the structures on section are given in Part II of this paper. The 
remnant of the embryonic vein bears a relation to the replacing 
perivenous lymphatic channel which is exactly the same as that 
of a collapsed inner tube to the enveloping shoe of a pneumatic 
tire. The inner skin of the shoe and the rim of the wheel represent the lymphatic inlimal endothelium. The space between the 
shoe and the collapsed inner tube is the lumen of the future 
lymphatic channel. The empty inner tube itself is the decadent 
embryonic vein upon and around which the secondary lymphatic 
channel is built. In the course of further development the venous 
remnant disintegrates and disappears, leaving a clear lumen for 
the lymphatic vessel, which thus completely replaces the earlier 
vein and comes to occupy absolutely the topographical position 
of the latter. 

Often the replacing lymphatic begins as an extraintimal 
channel partially surrounding the receding vein. This leads 
in course of further development to an expansion of the lymphatic 
channel not concentric with the axial line of the shrinking vein. 
The remnant of the vein then retires to a point on the intiiiial 
surface of the new lymphatic channel, and appears to project 
into the lumen of the latter. The resulting histological picture 



RELATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 



29 



will depend on the plane of section in reference to the course of 
the lymphatic and its contained venous remnant. Thus, as 
shown in the following schema, many sections give the appearance indicated in 1. If the plane of section should, however, lie 
in the line A B,it will divide the shrinking vein (4) and the enveloping lymphatic (5) in such a way as to produce the picture shown 
under 2. In other cases the lymphatic spaces unite around 
the entire circumference of the abandoned venule, and the lumen 
is then contained for long distances entirely within the lumen 
of the replacing lymphatic channel. 





The process just described is remarkably constant and uniform 
in the critical stages of mammalian lymphatic development. 
As can be readily seen in following the individual sections in 
the microphotographs published in PSart II, the significance of 
the conditions here shown is unmistakable. This is not a haphazard process, observed only occasionally, in a limited number 
of embryos, and then only in single sections, or, at most, in a few 
successive sections. In any average embryo of the proper age 
the same structures appear regularly in the same situatioi^s and 
in identical relationship to the embryonic environment. It is 
often possible, as the microphotographs and the corresponding 



30 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

reconstructions herewith published clearly show, to trace the 
forming Ijrmphatic withits atrophied vein kernel for long stretches, 
and in different embryos of approximately the same crown-rump 
measure the consistent repetition of identical histological pictures 
is remarkable. 

There are, of course, as in the ontogeny of other structures, 
individual cases of variation in which systemic lymphatic development is either more advanced or more retarded than is normal 
for the average of any given stage. But if a large nmnber of 
embrj^os of each typical period are examined and compared, the 
average standard of extraintimal lymphatic development attained 
by the majority of individuals in each stage is remarkably constant and uniform. 

The earliest stage in which I have encountered this typical 
replacement of an early embryonic vein by a perivenous extraintimal lymphatic is presented by certain 12 mm. cat embryos along 
the caudal circumference of the azygos-precardinal confluence. 
In the concavity of the azygos arch on each side, as this vessel 
turns ventrad to join the precardinal vein, these earliest evidences 
of the extraintimal replacement of preceding embryonic veins 
by independent perivenous lymphatic spaces are encountered. 
Thus, fig. 10 shows a section of this region in a 12 mm. cat 
embryo (series 217, slide x, section 12). Here the typical picture of the central collapsed core of the earlier vein (4) , enveloped 
by the clear extraintimal lymphatic space (5), is plainly to be seen. 
Fig. 11 shows the same region in another 12 mm. embryo (series 
211, slide X, section 15). Both the degenerating venule (4) 
and the enveloping lymphatic (5) are larger than in the preceding series, and occupy the same position between aorta (7) 
and left precardinal vein {6). 

In a 14 mm. embryo (series 127, slide viii, section 12, fig. 12) 
the section passing just caudad to the junction of left azygos 
(6) with left precardinal vein {6) shows these early lymphatic 
spaces (5) and their relation to the contained venous remnant (4) 
fully developed. Only one of the areas is denoted by leaders 
in the figure, but two equivalent areas are seen further dorsad 
and nearer to the ventral aspect of the azygos arch. The lym


RELATION OF LYMPHATIC TO BLOOD- VASCULAR SYSTEM 31 

phatic plexus, as development proceeds, from the 12 mm. stage 
on, approaches the large venous trunks more and more, until 
the spaces lie in direct apposition with the same, and unite to 
form the lymphatic trunk eventually destined to replace the left 
azygos arch and adjacent position of the left precardinal vein. 
This trunk then constitutes the cephalic end of the bronchomediastinal duct (37). Thus figs. 13 and 14 show two sections 
through the same region in a 15 mm. embryo (series 219, slide 
xiv, sections 19 and 16). Compared with the 14 mm. embryo 
the left azygos vein shows a marked reduction. The lymphatic spaces have enlarged and present a clear lumen on 
section, the remnant of the earlier vein, around which they 
developed, having disappeared. The spaces lie between aorta 
and left precaval vein, in close approximation to the dorso-medial 
circumference of the latter. The azygos segment of the thoracic 
duct (36) is seen dorsal to the interval between aorta and oesophagus, and ventral to the scant remnants of the earlier interazygos 
venous anastomosis {16). 

The reconstruction of a 15 mm. embryo (series 218) shown in 
fig. 170 in Part II, gives a clear idea of the extent and relations of 
this lymphatic complex (37) in this stage. 

B, Partial replacement of portions of the territory of an early 
embryonic venons pathway by an extraintimal lymphatic vessel, both 
venous and lymphatic channels either persisting side by side up to 
later developmental periods, or forming correlated components of 
the permanent adult vascular organization. 

The developmental processes just described appear most clearly 
marked in the earlier stages, and in connection with temporary 
embryonic channels and plexuses which are destined to undergo 
rapid degeneration and ultimate complete elimination. In the 
case of the embryonic veins which are retained for a longer period, 
or carried over into the permanent adult organization, the histogenetic stages of lymphatic development are identical in kind, 
and differ only in degree from those just detailed. In place of 
complete replacement of the antecedent vein by the lymphatic 
channel, this replacement is only partial and leads to the typical 



32 DEVELOPMENT OP THE SYSTEMIC LYMPHATIC VESSELS 

close parallel association of lymphatic and venous vessels so 
characteristic of the later embryonic stages and of the permanent adult pathways of both the lymphatic and the venous 
systems. 

Figs. 15 and 16 show transverse sections of a 14 mm. embryo 
(series 222, slide vii, section 26, and sUde viii, section 4) in the 
region of the external jugular vein. The lymphatic spaces (;87') 
are in full development, and are applied chiefly to the medial 
aspect of the plexus of the external jugular vein (27). The lymphatic endothelium is clearly marked. 

Fig. 17 shows a transverse section in the upper thoracic region 
of another 14 mm. embryo (series 37, slide xiii, section 12). A 
typical lymphatic anlage (53) is applied to the medial wall of the 
left precaval vein. 

Fig. 18 shows a transverse section through the mid-thoracic 
region in a 17 mm. cat embryo (series 258, slide xviii, section 
9, X 225). 

The extraintimal anlagesof the thoracic ducts (S6), which usually 
in thisstage have advanced to the production of a continuous and 
uninterrupted channel system, are seen on each side closely applied to the ventral aspect of the left and right azygos veins. 
The latter are in the height of their development, forming large 
and symmetrical longitudinal venous trunks (S, 6) connected by 
the supra-aortic interazygos anastomosis. In course of further 
development the left azygos vein and the interazygos anastomosis 
are destined to undergo progressive reduction until they are 
eventually entirely lost. Their topographical position is then 
occupied by the replacing left segment of the thoracic duct complex (36). The right azygos vein, which is carried as a permanent vessel into the adult organization, also undergoes considerable relative reduction, correlated to the corresponding increase 
in the caliber of the main (right) segment of this portion of the 
thoracic duct complex. 

The beginning of this process is seen well in fig. 19, which shows 
a transection of the same region in a 19 mm. cat embryo (series 
253, slide xxiv, section 9, X 225). The change from the preceding 



RELATION OF LYMPHATIC TO BLOOD-VASCtJ LAR SYSTEM 33 

stage (fig. 18) is marked both in the venous and the lymphatic 
channels. The former are relatively much reduced, while the 
latter have correspondingly increased in extent. The azygos is 
mainly represented by the right channel (S). The left channel (6) 
has become small, but is still connected by the transverse interazygos anastomosis (15) with the larger and permanent right 
trunk. The right thoracic duct (36) is likewise large. A dorsomedial extension of the same, which carries into the interval 
between aorta and interazygos plexus, will, in later stages, replace 
the latter secondarily, after the complete recession of the left 
azygos vein. The left thoracic duct {S6) is also of large size and 
fills a considerable part of the area formerly (fig. 18) occupied 
by the left azygos trunk. Some decadent remnants of the ventromedial azygos plexus (4) are still seen associated with the left 
duct, and are in process of replacement by a lymphatic space (5) * 
destined to make connection between the left thoracic duct anlage 
and the mesenteric lymphatic plexuses (cf. p. 148, figs. 266 to 
270, 51). 

Figs. 20 to 24 show transverse sections in the region of the developing mesenteric lymphatics and of the ascending lumbar lymphatic trunks in a 17 mm. embryo (series 258, slide xxiii, sections 
34, 33, 32 and 31.) The embryonic veins (74) occupying the root 
of the mesentery caudal to the subcardinal cross-anastomosis are 
in the process of being replaced by extraintimal lymphatic spaces 
. {61) which are destined to become confluent and form the anlage 
of the future mesenteric lymphatic sac. 

The region in question is not only interesting in reference to 
the ontogenesis of the abdominal lymphatic sacs and channels, 
but the arrangement of the periaortic axial venous trunks and 
their relation to the developing lymphatics is, in combination with 
the next following stage (20 mm., figs. 25 and 26), of the highest 
importance in interpreting the phylogenetic relations of the main 
abdominal veins in mammalia. For these reasons a somewhat 
more detailed consideration of the sections may properly be introduced here. 

Fig. 20 shows section 34 of slide xxiii of series 258 in a magnification of 75 diameters and affords a comprehensive picture of the entire 



34 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

topographical field involved. The strands of the sympathetic (l) 
are supra-aortic. On each side of the aorta (7) are the large and symmetrically developed right and left postcardinal veins (67 and 68) , 
with the ascending tninks of the ilio-lumbar arteries (A.ilid-lumb. 
transv. ant.) (not labelled in the figure) applied to their ventrolateral circumference. The subaortic area shows the cross-sections 
of four symmetrical vascular channels, two venous and two lymphatic. Immediately venti alto the aorta, and closely applied to 
its ventral wall and to each other, are two longitudinal parallel 
axial veins which are connected at intervals by a few short transverse anastomoses. These vessels are the temporary and very 
evanescent homologues in the placental embryo of the channels 
which McClure'® has described as the "cardinal collateral trunks'* 
in the embryo of Didelphis marswpialis, and from which he has 
traced the development of the preaortic postcava characteristic 
of the Marsupalia. These vessels are derivatives from the earlier 
preaortic cardinal-subcardinal venous plexus below the crossanastomosis, but differentiate in Marsupials along separate and 
distinct axial lines. They are destined, as are the corresponding 
portions of the subcardinals proper, to be entirely replaced in the 
typical placental development by the chain of preaortic lymph 
channels and nodes, but are capable, in aberrant types among the 
placentalia, of yielding, by further and continuous development, 
a type of preaortic postcava which in every respect corresponds 
to that encountered in Marsupials. McClure^* has described this 
condition in Tragulus, and his observation has been confirmed 
in a number of dissections by Beddard and others. The fortunate 
acquisition recently of a series of Tragulus embryos, through the 
kindness of the officials of the Smithsonian Institution, has enabled 
my associate Tilney to trace, in a publication now in preparation 
for the press, the development of the venous and lymphatic 
systems in this aberrant ungulate in their mutual interdependence, 
and to show the correspondence of the venous genetic processes 

•• C. F. W. McClure: "The Anatomy and Development of the Postcava in 
Didelphis marsupialis/' Am, Jour. Anat,, vol. v, 1906. 

" C. F. W. McClure: "The Postcava of an Adult Indian Chevrotain {Tragulus 
meminnaj Erxleben). Anal, Anz., Band, xxix no. 13 and 14, 1906, pp. 375-377. 



36 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

persistence and further development of the cardinal collateral 
veins. In other words, not a single individual in the entire seiies 
possessed a marsupial postcava, although every shade in the possible range of variation in the district of the post- and supracardinal 
lines was represented by numerous examples. Thus with an abdominal venous organization of very unstable equilibrium, as shown 
by the large percentage of cardinal variants,^^ the cat yet keeps 
entirely within the district of the common genetic ground plan 
assigned to the placentalia. This phylogenetic consistency is 
maintained in spite of the fact that, as just demonstrated in series 
258, the embryo develops the raw materials, as cardinal collateral 
channels, out of which a preaortic postcava of the marsupial 
type could be evolved. In my own estimation cats possessing this 
form of postcava may exist and may eventually be found. But 
the failure to encounter them in the relatively large series of adults 
already examined speaks volumes for the value of vascular organization in interpreting phylogenetic relations. 

In this light the postcaval development and adult structure of 
Tra^ulus, for example, are of the utmost importance and significance. The unprejudiced observer is often forced to wonder 
why'some exponents of palaeontological research are content to 
draw far-reaching phylogenetic conclusions from the remnants of 
the incomplete locomotory apparatus at their disposal, without 
utilizing the results of modern comparative anatomical and embrj'ological investigation in determining at least the mutual relations 
of the extant forms, massed by an ironclad taxonomy into more 
or less questionable groups, whose ancestry and derivation form 
one of the primary problems of the palaeontologist. The case of 
Tropins just alluded to, the parotid complex and alimentary 
canal of Hyrax, the amniote homologies of the derivatives of the 
Sulcus buccalis determined by Schulte, the sharp line of lymphatic 
demarcation recently shown by Silvester to structurally separate 
absolutely the platyrrhine and catarrhine divisions of the lower 
primates, these and other facts are only instances in which the 
inadequacy of a superficial convergence of dental and skeletal 
characters, for the purpose of establishing valid phylogenetic 
relations, is revealed by cardinal divergence in the far more stable 
and important organization of vascular and visceral structure 



RELATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 37 

The prevalent lack of coordinate deduction between vertebrate morphology and palaeontology is accentuated by contrast 
with such publications as Weber's ''Saugethiere'' and, more 
recently, W. K. Gregory's ''The Orders of Mammals", based 
largely on the author's joint work with Osborn, and on the latter's 
previous classical researches, and published by the American 
Museum of Natural History (Bulletin, vol. 27, February, 1910). 

Workers in the general field of vertebrate structure appreciate 
fully the immense practical value in their own special investigations of books of this type, in which, to quote Gregory's words, 
''the data of sj^stematic mammologj', of comparative anatomy 
and embryology shall ultimately be integrated with the data of palaeontology, to the great advantage of these now more or less 
independent lines of study." 

In embryo 258 (fig. 21) the space ventral to the cardinal collateral veins and the ascending lumbar lymphatic trijnks, is occupied by a plexus of mesenteric lymphatics (61) draining into 
the latter. On each side are seen sections of the ureter {68) y and 
further laterad of the iliac vessels (61), Ventral of the intestine 
{6S) are the Wolffian ducts (64) and the cloaca (63) j with the 
hypogastric arteries (66) laterally. 

Fig. 21 shows the important central vascular region of the same 
section in a magnification of 150 diameters. The relation of the 
cardinal collateral trunks (74.) to the ascending lumbar lymphatics 
(7S), and of the latter to the postcardinal veins (67 y 68) can be 
more clearly seen. The lumen of the mesenteric lymphatics 
(61) still contains in places remnants of the decadent venous 
plexus around and upon which they developed as replacing extraintimal spaces. 

The three succeeding sections, tracing the structures caudocephalad, are shown in figs. 22, 23 and 24, all in a magnification 
of 150 diameters. The connections of the lymphatic channels 
developing along the iliac vessels with the ascending lumbar 
trunks are especiall}^ well seen on the left side of the three figures, 
also the anastomoses between the two cardinal collateral veins in 
figs. 23 and 24. 

Figs. 25 and 26 show transverse sections of the hinder end of the 
bodv in a 20 mm. embrvo (series 241). 



38 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

Fig. 25 (series 241, slide xxx, section 4) gives, in a magnification of 76 diameters, a topographical view of the entire field. 
This stage, compared with the preceding 17 mm. embryo, is marked 
by the full development of the supracardinal venous line, responsible for the production of the greater portion of the typical 
adult placental postcava below the renal level, and by the correlated development of the supra- or retro-aortic lymphatic 
sinuses associated with the same. 

The periaortic area in fig. 25 gives a ijlear view of the vascular 
relations and of the postcardinal and supracardinal axial venous 
trunks. 

The former {67 , 68,) are seen on each side, between aorta (7) 
and metanephros {65), receiving the veins from the mesonephroi 
in whose dorso^-medial border they are lodged. 

The latter {59, 60) lie dorsal to the aorta (7) between this vessel and the sympathetic strands {1 ) . 

The right supracardinal {60) has already gained the ascendency 
and is in process of establishing the channel of a normal right 
retro-aortic postcava, which is the typical vein for the cat. The 
correspondingly reduced left supracardinal {59) occupies the same 
situation on the left side. Associated with the supracardinal 
venous channels are the supracardinal lymphatic trunks {76), 
which form the anlages of the main adult retro-aortic lymphatic 
plexus. These develop as extraintimal spaces replacing portions 
of the earlier supracardinal venous reticulum. In accordance 
with the normal type of development observed in this individual 
embryo, the large permanent supracardinal (postcaval) vein of 
the right side is accompanied by a relatively small lymphatic 
channel {76 right), while on the left side the much reduced left 
supracardinal {59) is already nearly replaced by the corresponding lymphatic vessel {76 left) . In course of further normal development this replacement will become complete and then the 
area formerly occupied by the left supracardinal vein will be 
entirely filled by the substituted large left retro-aortic lymphatic. 
The permanent functional venous channel of the right side {60) 
on the other hand, developing into the typical placental postcava, will be accompanied by a relatively small right lymphatic 



KBLATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 39 

• 

trunk following its dorso-lateral aspect. As will be shown later 
(Part v.), departures from the normal type of venous development in this region, and the substitution of other embryonic 
pathways for the right supracardinal in building up this section 
of the adult postcava, produce corresponding and correlated 
changes in the arrangement of the main retro-aortic lymphatic 
channels. 

Fig. 26 shows the periaortic region of the same embryo, further 
caudad, in a magnification of 150 diameters (series 241, slide 
XXX, section 14.) The section is taken at the level of a pair of 
dorsal intersegmental arteries which pierce the supracardinal 
venous (5S, 60) and lymphatic {76) complex, and divide the vein 
of the right side into two components {60, 60) . Further ventrad 
the two postcardinal veins {67, 68) are seen, already considerably reduced, ventrolaterad to the ureters {58) and the accompanying ascending lumbar lymphatic trunks {75). The connection of the latter with the supracardinal lymphatic channel is 
especially clear on the right side of the embryo. 

Taken together, the 17 mm. and 20 mm. embryos just figured 
and described afford a very clear and comprehensive picture of 
venous and lymphatic development in their mutual relationship 
in this region. 

The schematic text figures A, B and C may help to explain 
this relationship. 

Fig. A is based on the joint studies which McClure and I made 
on the development of the postcava in embryos of the domestic 
cat. The figure was demonstrated to the 21st Session of the 
Association of American Anatomists in 1906 at the time of presentation of the communications, although not reproduced in the 
brief abstracts of the papers subsequently published.**' ^^ 

The figure represents a composite schema of the main periaortic venous axial pathways of the abdominal region. These 
pathways developing along diefinite and constant axial hydrostatic lines out of the periaortic venous reticulum, have all been 
determined by us in embryos of the cat. They do not, of course, 
all coexist at the same time in any embryonic stage, but normally 
succeed each other in definite sequence. The entire range of 



40 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

extensive variations in the domain of the adult postcava of the 
cat can be clearly interpreted genetically^* on the basis of 
this common groundplan, through abnormal persistence of one 
or more of the embryonal pathways usually destined for complete 
obliteration, thus producing farreaching modifications in the 
structure and relations of the resulting atypical postrenal seg
 

ment of the adult postcava. 

This periaortic axial venous lattice with connecting transverse branches (Fig. A) contains four components on each side, 
which develop in the following order: 

1 . The postcardinal veins (1 ) . 

2. The subcardinal veins (£), 

3. As secondary derivatives of these two veins, the preaortic 
cardinal collateral channels (S). 

4. As secondary dorsal derivatives of the postcardinal trunks, 
the supracardinal veins (4)
In the course of normal venous development along the line 
typical for the great majority of placental mammals the right 
supracardinal vein (4) obtains the preponderance and furnishes 
the postrenal segment of the adult postcava, thus freeing the 
ureter from its primitive retro-venous position. 

A part of the early capillary periaortic reticulum, out of which 
this vessel develops, is secondarily replaced by extraintimal 
lymphatic spaces, which through their confluence form the relatively small retro-aortic lymph channel (40 > following in the adult 
the dorso-lateral circumference of the postcava (4). (Figs. B and 

n. 

The right and left postcardinal veins (1) are in part retained 
as the terminals of the sex veins, in part replaced by the accompanying lymphatic trunks (i')- (Figs. B and C). 

The left supracardinal vein (4), and both subcardinal veins 
(j?) , below the cross-anastomosis, as well as both cardinal collateral veins (S), retrograde and are entirely replaced secondarily 
by lymphatic channels. 

The lymphatic replacing the left supracardinal vein (40 forms 
normally in the adult the main retro-aortic lymphatic sinus. 
(4'i left, in figs. B and C). 



42 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

The lymphatic channels replacing the subcardinal and cardinal 
collateral venous trunks fonn the extensive system of the adult 
ascending lumbar and preaortic lymphatic vessels and nodes 
(2' and S' in figs. B and C). 

Of course it is quite apparent that the adult placental differentiation occurs in the district of the post- and supracardinal 
lines, with a strong predilection for the right supracardinal as 
the main path of the postrenal segment of the adtdt postcava. 
It is equally apparent that in correctly valuing the significance 
of the departures from the normal type of placental postcava 
all four of the available components, viz., right and left postcardinal and right and left supracardinal lines, must be taken 
into account as potential factors in the development of the atypical placental postcava. The relation of the veins to the ureter 
will then decide the question of the genetic derivation, as being 
either the persistent postcardinal or supracardinal channel of either 
the right or left sides, in the case of single trunks, or of both sides 
in instances of double bilateral adult channels. 

Thus all the recorded cases of variant postcaval veins of the 

cat, and of man, can be clearly interpreted on this basis, as has 

been done by McClure, Darrach and myself in previous publications.2»'24,26 

Furthermore, the placental types in which a normally so-called 
double postcaval vein occurs, as, e.g. in some of the aquatic 
carnivores, some insectivores and edentates, are readily led back 
to persistence of both right and left axial channels with absence 
or reduction of the iliac anastomosis. Again the position of the 
ureter in reference to the bilateral trunks will characterize each 
of them as being either post- or supracardinal in derivation. 

In the marsupials McClure's researches already quoted,'^ 
show clearly that the members of this subclass depend upon the 
continued development of the ventral preaortic venous pathways (^, S) of the common vertebrate groundplan (fig. A) for 
the evolution of their typical ventral preaortic postrenal segment of the postcava, with consequent reduction of the postcardinal line (1) to the r61e of a sex vein terminal, and the complete 
suppression of the typical placental supracardinal lines (4) in most 



44 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

with the same. Nowhere is there any suggestion of a bud or an 
outgrowth from the vein as forming the origin of these lymphatic 
spaces. It now remains to clearly prove the genesis of these 
spaces, and to trace their growth from their inception up to the 
stages just pictured in which fully organized Isonphatic and venous channels lie side by side in the mutual relation above figured and described. The proof of their origin is furnished by the 
series of microphotographs of successive sections of the earlier 
stages given in Part II of this communication, in connection with 
the individual series described and figured in tracing the development of the preazygos and azygos portions of the thoracic ducts. 
The microphotographs, and especially the reduced reproductions 
figured, are not so clear as the actual preparations, because focal 
adjustment is required to follow the endothelial lining of the 
spaces in their entire circumference, and because they lack the 
differential stain of the sections. Still they are sufficiently distinct to establish definite conclusions. Merely referring, therefore, at this time to the following detailed illustrations, the general 
topic of extraintimal replacement of embryonic veins by lymphatic spaces and the character of the latter deserve some further 
consideration. 

The lymphatic anlages, as above stated, if studied under sufficiently high power and with some care, are seen to begin as intercellular clefts in the periaortic mesoderm, adjacent to the postcardinal venous plexus, and chiefly on its ental aspect, between it and 
the aorta. 

The individual lymphatic spaces, at first small and separated 
from each other, enlarge, elongate and become confluent, to form 
larger continuous channel segments, while innumerable newly 
formed spaces of the same character appear in the surrounding 
tissue, join with each other, and with the earlier preformed lymphatic channels, in exactly the same manner, and with the same 
appearance of lymph endothelial '* budding'' or *' sprouting" as 
is observed in haemal vascularization of new areas by the junction 
of the earlier blood capillary anlages with secondary haemal 
plexuses. In these later ^ages the veins are surrounded by a close 
lymphatic plexus, which, however, does not as yet form a con


RELATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 45 

nected channel system, but is composed of longer and shorter 
segments still independent of each other. 

These finally become confluent, to form the main systemic 
lymphatic collecting trunks, and then onlj'' do these establish 
their final junction with the jugular lymph sacs, through whose 
interposition, as above stated, they gain in the typical mammal 
their permanent entry into the venous system. 

In this ontogenesis of the systemic lymphatic vessels certain 
relations between them and the venous system deserve further 
notice. 

In the early stages the lymphatic mesenchymal spaces form a 
wide meshed network (cf. series 111, figs. 1 to 7, series 120, figs. 
8 and 9). There is thus a marked similarity in the earliest stages 
of both the haemal and the lymphatic vessels, for the peripheral 
venous embryonic pathways are in their corresponding stages likewise still largely in the condition of a capillary reticulum. As the 
main lines of venous drainage crystallize out of the antecedent 
plexiform arrangement, the adjacent enlarging lymphatic channels 
crowd in on the condensing venous line and continue the close relationship which the earliest lymphatic anlages maintain to the 
adjacent veins. Thus the main embryonic venous channels develop along certain definite hydrostatic lines by enlargement and 
confluence of the individual plexiform elements of the indefinite 
antecedent network occupying these lines. The capillaries outside of these lines retrograde, so that the area of crosssection of 
the defined venous channel is less than the cross-cut area of the 
plexiform network which it replaces.- '^ 

The distinct impression is given that the space thus vacated 
by the condensation of the plexiform venous network of the earlier stages affords to the replacing lymphatic plexus the opportunity for greater growth and expansion, and that subsequently, 
in repetition of the process previously active in the venous reticulum, the lymphatic network condenses in a similar manner into 
more defined channels along similar hydrostatic drainage lines, so 
that the newly established main lymphatic vessel now closely 
follows the main venous channel. It is to be noted, however, 
that this organization of main vascular channels is usually less 



46 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

complete in case of the lymphatic vessels, as compared with the 
corresponding vein. The lymphatic system retains, much more 
perfectly than the venous, in many situations the original embryonic plexiform type. 

At first the cells limiting the earliest lymphatic spaces are of 
the usual irregular cuboidal form. As the spaces enlarge, open 
out and thus become better defined, the limiting mesodermal cells 
become flattened, and finally assume a typical endothelial character and form. Thus, for example, the endothelial lining of the 
primitive mesodermal lymphatic spaces {77) is more clearly developed in the 10 mm. embryo, series 120, shown in figs. 8 and 9, 
than in the corresponding sections of embryo 111, of the same 
crown-rump measure (figs. 1 to 7). The former embryo is slightly 
in advance of the latter as regards the development of the parietal endothelial lining of the primitive mesodermal intercellular 
lymphatic spaces. In some instances a few modified mesodermal 
cells intervene between the cells limiting the lymphatic spaces 
and the endothelium of the adjacent venous radicle. In others 
no such intervening cell-layer exists, and the lymphatic space is 
separated from the venous lumen only by the latter's endothelial 
wall. In other words, in the extent of the lymphatic anlage, a 
single-celled membrane furnishes a part of the venous intima and 
at the same time contributes to the endothelial definition of the 
lymphatic space. This relation of vein and lymphatic anlage is 
shown very clearly in fig. 17. The lymphatic space (5S), which is 
closely applied to the medial wall of the left precardinal vein, is 
only separated from the lumen of the latter by the endothelial 
membrane which serves to line both spaces for the area of their 
mutual contact in this stage. Subsequently, with the regression 
of the left precardinal vein, this lymphatic anlage will correspondingly enlarge to form an extensive lymphatic plexus, which will 
eventually topographically replace the vein along which it arose. 
In order to briefly characterize this relation between vein and 
lymphatic, McClure and I defined in an earUer publication*^ these 
spaces as the ''Extra-intimal" anlages of the systemic lymphatic 
vessels, with due regard to the relation existing between them and 
the intimal endothelial lining of the embryonic veins. The mechan


RELATION OF LYMPHATIC TO BLOOD- VASCULAR SYSTEM 47 

ical concept involved in this term seems, to judge from a recent 
publication,'' to have been difficult to acquire. I am glad to be 
able to make myself clear by reference to fig. 17, where the mutual 
relation of the two vascular lumina is evident without further 
description, and to the numerous detailed illustrations on a larger 
scale of magnification which accompany the account of the development of the thoracic ducts in Part II of this communication. 

By far the larger number of the early lymphatic channels are 
the product of fusion of these ''extra-intimar' spaces, and hence 
closely follow the veins of their respective regions. Subsequently, 
with the development of a venous adventitia, this relationship 
is somewhat altered in case of those veins which are included in 
the permanent venous organization. The close relation existing, 
however, throughout Ufe between these veins and the accompanying lymphatics is based on this intimate primitive association of 
their respective anlages. 

On the other hand, the extra-intimal position of the earliest 
lymphatic spaces furnishes the explanation of another relation 
manifested between the developing systemic lymphatic channels 
and those embryonic veins which in course of normal venous development are destined to undergo reduction and finally complete 
suppression, when the primitive bilateral and symmetrical venous 
system of the earlier embryonic stages shifts to the dextral assymmetrical type of the main adult axial channels. In these 
circimfistances the systemic lymphatic vessel associated with the 
temporary embryonic vein experiences, apparently through the 
shrinkage of the latter, an impetus to its own more extensive development, so that it comes to occupy in general topographically 
the space filled by the vein in the earUer stages. 

Thus the embryonic period which marks the normal ontogenetic 
swing of the main venous line to the right through the secondary 
sinistro-dextral iliac, hemiazygos and brachiocephalic cross anastomoses, sees the simultaneous increase in the corresponding lymphatic channels of the left side, which topographically replace the 
abandoned left embryonic venous pathways of the earlier and sym
» Sabin: Anal. Rec, vol. ii, 1908, p. 50. 



48 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

metrical stage. This occurrence leads to the well-known relative 
location of the main axial veins and lymphatics in the normal 
adult, in which the lymphatic vessels are chiefly situated on the 
left side and form, so to speak, a mirror-picture of the right sided 
axial venous channels. 

Fig. 27 shows the reconstruction of the anterior venous and 
lymphatic complex in a cat embryo of 18 mm. (series 88) in the 
ventral view, and fig. 28 of the same preparation in the lateral 
aspect from the left side. The brachiocephaUc cross anastomosis 
is already well under way, resulting in a marked diminution of 
the left anterior caval vessel and a corresponding increase in the 
permanent right anterior cava or right duct of Cuvier. Conversely, the lymphatic vessel accompanying the diminishing left 
precaval vein is of large size, while that applied to the massive 
right precaval is comparatively small. 

This principle of lymphatico-venous replacement, indicated 
clearly in the later embryonic stages, is strikingly illustrated in 
the adult. Thus, for example, the adult cat presents normally 
the arrangement of the great veins of the head and neck which 
is so frequently encountered in mammals below Primates, in 
which the large embryonic internal jugular vein is much reduced 
or even entirely obliterated, while secondarily the external jugular vein has assimied the function of the main vessel. Under 
these normal circumstances the lymphatic trunk accompanying 
the minute internal jugular vein or, in case of its entire default, 
occupying its position, is well developed and the largest element 
of the entire cervical lymphatic complex, while the external jugular vein is, on the other hand, accompanied usually by two very 
slender lymphatic vessels. 

In instances, however, in which the embryonic proportion 
between the two jugular veins is retained in the adult, so that the 
internal jugular appears as a large and functionally important 
vessel, while the external is correspondingly diminished, the internal jugular lymphatic trunk is reduced, while the double lymphatic 
vessel along the external jugular is enlarged, and evidently acts 
in compensation in the cervical lymphatic return. 



RELATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 49 

Again, in the same way, in adult animals with normally placed 
right postcava, the main supracardinal lymphatic trunk, draining 
the abdomen and the posterior extremities, follows the left side of 
the large artery. 

In the not infrequent instances, however, of left sided postcava 
or postcardinal vein in the adult the reverse obtains, and the periaortic lymphatic channels predominate on the right side and occupy the place usually filled by the large vein in normal venous 
development. 

I have encountered in the adult series so far examined no instance of persistent left precava replacing functionally the normal 
right superior cava, but have no doubt that this venous variation 
would involve a transposition of the proximal end of the thoracic 
duct to the right side, or at least a marked increase in the size and 
functional importance of the usually insignificant preazygos segment of the adult right lymphatic duct. 

The developmental outline just given describes the mutual 
ontogenetic relations of the venous and lymphatic systems throughout the greater part of the body. 

Systemic lymphatic development in these regions is, however, 
by no menas confined to the immediate environment of degenerating embryonic veins. The same field, which shows the above 
described histogenetic processes in the development of extraintimal lymphatic spaces surrounding and replacing a decadent 
venule, will at the same time contain numerous equivalent lymphatic mesenchymal clefts and spaces which continue to develop 
independently of any association with retrograding veins. Naturally, these independently developed early lymphatic anlages 
are less striking than those above described as developing in association with a receding vein. They are smaller, because they 
lack the bulk of the contained venous core, and they are more 
difficult to clearly differentiate against the surrounding mesenchyme. They are, however, always present and their eventual 
connection with the larger perivenous lymphatic spaces can be 
ascertained definitely by following their development through 
the proper stages. 



50 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

In additioD, in certain areas, a small group of the earliest lymphatic anlages appear to develop in the mesenchyme along definite Unes, and in distinct patterns, but v^ithout any preceding 
venous reticulum. They impress me, for example, in the area 
surrounding the omphalomesenteric artery, as systemic lymphatic 
channels developing ia the placental embryo in regions which are 
no longer ontogenetically the seat of venous development, although occupied by vei 3S in other mammalian types. Thus the 
cardinal collateral line of the marsupials^'^ and the correlated 
venous area of the monotremes" no longer develops as a permanent veoous plexus in placentalia'* but only partially appears 
in certain fonns as a temporary and evanescent component of 
the abdominal venous complex, as described above for certain 
stages in the development of the cat (pp. 29 to 33 and figs. 20 to 24) . 
Its place, however, is partially occupied by an early lymphatic 
plexus de\ eloped in the preaortic mesoderm from the omphalomesenteric anlages caudad. Here we are apparently dealing with 
an instance in which general phylogenetic venous lines have been 
almost or entirely abandoned in favor of other pathways. 
Such lines appear, however, to be retained under these conditions in the lymphatic organization. Thus, the spaces just 
referred to, as will be shown subsequently, form the first inception of the extensive network of lymphatic vessels which in the 
adtdt cat surrounds the aorta and the origin of the superior 
mesenteric artery, closely interwoven wdth the semilunar sympathetic and the adrenal plexus, and connecting on the one 
hand with the portal and intestinal lymphatics, and on the other 
with the beginning of the thoracic duct. This adult mammalian 
lymphatic plexus forms a perfect lymphatic shadow-picture of 
the lacertilian ontogenetic peri-omphalomesenteric venous ring. 

In conclusion, I wish to give briefly a simunary of my reasons 
for regarding the structures described in this communication as 
the anlages of the systemic lymphatic vessels. 

** Except, as recently determined, in Tragulus, in wnich Ungulate the adult 
postcaval system is of the marsupial type, and in certain embryonic stages of the 
Cat (15.5-17 mm.) in which the channels appear as evanescent preaortic vessels, 
subsequently entirely replaced by lymphatics. (Cf. series 258; figs. 20 to 24.) 



• • •• 

• • : 






• 



•• t • • • 

• • "• • •• • 

• • • • • • • 

• • • • * • • 



RELATION OF LYMPHATIC TO BLOOD-VASCULAR SYSTEM 51 

These early lymphatic anlages, whether formed independently 
in mesoderm, or on the site of phylogenetically abandoned venous 
Unes, or, as is generally the case throughout the body, in close 
correlation to the embryonic venous pathways, always appear 
in the same situations and, in the average embryo, at the same 
developmental period. Their constant character, and regular 
occurrence and relations, repeated within very narrow limits of 
individual variation in every embryo of the proper stage, imparts 
to them a definite morphological character. In every series of the 
proper age in my collection I find the same spaces in the same 
place and in identical relationship to the adjacent veins. In some 
individuals, as above stated, they develop earlier than usual, in 
others their appearance is retarded, but this applies only to the 
achievement of the full development typical for the average embryo 
of a given stage. In the retarded individuals the same structures 
are always present, only they are less strikingly developed and less 
niunerous when compared with the average normal type characteristic of the period under consideration. With sufficient magnification it is not difficult to distinguish sharply between the 
perihaemal lymphatic spaces and the blood-vascular channels 
proper. 

With sufficient material every stage of their development can 
be followed up to the confluence of the entire system and its final 
entrance into the jugular lymph sacs. 

These spaces are neither artefacts due to embryonic shrinkage, 
nor are they the unfilled portions of the blood-vascular capillary 
network. They are, on the other hand, the well-defined earliest 
anlages of the systemic lymphatic vessels. The more perfect, as 
a matter of fact, the embryonic fixation is, the more clearly can 
these structures be indentified under the microscope. Their 
history, as will be shown presently, can be traced with the utmost 
accuracy, and they can be followed step by step in their development up to their inclusion in the completed and connected 
lymphatic channel system. 

But even in their earliest stages they possess an unmistakable 
and definite morphological character, quite as distinct as that 
of the adjacent blood channels. They can be followed closely in 



52 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

good serial sections of the proper thickness and fixation, and can 
be reconstructed in the same manner and with the same accuracy 
and certainty as the blood channels with which they are for the 
most part so closely associated, although their lumen connects at 
no point with that of the vascular channels. 

These statements are based, not on isolated observations, but 
on the close and repeated examination of a very large number of 
embryos of the same form. It seems curious to me that the presence of the first lymphatic anlages, as above described, should be 
denied, or, as has been recently done, that the isolated appearance of these spaces should be ascribed to the ''sudden collapsing " 
of a lymph vessel. At the time at which they make their first 
appearance there are no ''lymph vessels'' to "collapse," no more 
than there are in the homologous haemal ontogenetic stages bloodvessels in the sense of continuous channels. On the contrary, 
when they reach their period of most striking development (cat, 
13-14 mm.) these perivenous lymphatic spaces are, if anything, 
distended, not only by their fluid contents, but by the remnant 
of the embryonic atrophying vein which they are in the process 
of replacing. The only structure showing any sign of "collapse'' 
is the empty endothelial bag of the decadent venule. The spaces 
become relatively reduced in. size in the later stages, after the 
multiple separate early anlages have fused into a more continuous lymphatic channel system. 

These spaces are always present in embryos of the proper stages 
in the typical position and in constant relation to the venous 
channels. By following carefully and with suflBcient material 
their further growth and development in succeeding stages, a clear 
and consecutive picture of systemic lymphatic genesis is given. 

It is noteworthy, in view of the incorrect statements published 
to the contrary, that these primary anlages of the systemic lymphatic system develop constantly in embryos of the cat before the 
definite organization of the jugular Jymph sacs. These latter 
structures, in the 10 mm. cat embryo, are still largely in the condition of a perivenous capillary plexus, at a time when the first 
lymphatic anlages can be distinctly recognized in the axial 
mesoderm. 



54 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

2 The lymphatic endothelium is an independent modification of the mesodermal cells lining the first anlages of the lymphatic spaces, and is not derived from the haemal vascular 
endothelium. 

3 I am obliged to deny the assumption that the mammahan 
systemic lymphatic vessels arise by the confluence of numerous 
elements detached in course of development from the embryonic 
veins. 

4 I am obliged to put myself emphatically on record against 
the assumption that the mammalian systemic lymphatic vessels 
arise by a progressive sprouting from center to periphery fron) 
the endothelium of veins, or from that lining the jugular lymph 
sacs, or equivalent structures in other regions of the body. The 
mammalian embryo offers no evidence of such occurrences. 



PART I, PLATES 

FIGURES 1 TO 28 

The series here figured and de«oribed are in the embryological collection of 
Columbia University, with the exception of series 34, which belongs to the embryological collection of Princeton University. I am greatly indebted to Prof. 
C. F. W. McClure for the opportunity of studying this series and publishing the 
eight sections shown in figs. 245 to 251. 



FIGURE 1 

1 Transverse section of 10 mm. cat embryo (series HI, slide VIII, section 4), 
X 175*— Topographical picture of site of earliest lymphatic space development. 

1 Sympathetic nervo. 

8 Oesophagus. 

S8 Left postcardinal vein. 

69 Lungs. 

72 Right dorsal aorta. 

73 Left dorsal aorta. 

77 Mesenchymal intorccllular lymphatic anlages. 

78 Coelom. 



FIGURE 2 

2 Tranfiverre Mv-tion of 10 mm. cat embr>*o series 111. :«lide VIII. section 4) 
y 30O — left .siile of embrj'O. 

GS I^eft iK>sicarrlinal vein. 

73 I^ft dorsal aorta. 

77 Mesench\-mal intercellular h-mphatic anlafces. 

7S C'oelom. 

79 Coelomic stoma. 



FIGURE 3 



3 Same. X 600. 



FIGI'KES 4 AND 5 

4 Transverse section of 10 mm. cat embryo (series 111. slide VIII. section 6), 
X 300. 

5 Same, section 7, 



FIGURES 6 AND 7 



6 Same, section 8. 

7 Same, section 9. 



FKJl'RKS 8 AND {) 

S Trafisvprsc sorti<»n of 10 inni. cat embryo (series 120, slide IX, section 25) 
X .WO. 
Saiiie, seel ion 2r>. 

1 Syinpiithetic nerve. 

(iS Left posteanlinal vein. 

7.') Left dorsal aorta. 

77 Mesenehynial int<'reelliilar lymphatic anlages. 

78 Coeloni. 



FIGURES 10 AND 11 

10 Transverse section of anterior thoracic region of 12 mm. cat embryo (series 
217. slide X, section 12). X 225 — showing early extraintimal lymphatic development. 

11 Transverse section of anterior thoracic region in a 12 mm. cat embryo (series 
211. slide X. section 15). X 225. 

3 Prci-ardinal or precava. resp. azygos of right side. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 E.Ytraintimal or perivenous lymphatic space surrounding degenerating 

embryonal vein. 
Precardinal or precava, resp. azygos of left side. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 

10 Pulmonarv arterv. 
22 Vagus. 



FIGURE 12 

12 Transverse section of anterior thoracic region in a 14 mm. embryo (series 
127, slide VIII, section 12), X 225. 

4 Atrophying embryonal vein, forming kernel in interior of develop
ing and replacing lymphatic space. 

5 Ex train timal or perivenous lymphatic space surrounding degen
erating embryonal vein. 

6 Precardinal or precava, reap, azygos of left side. 
6' Left azygos vein, thoracic portion. 

7 Aorta. 

8 OosophagiLs. 



FIGURES 6 AND 7 



6 Same, section 8. 

7 Same, section 9. 



FIGURE 15 

16 Transverse section through lower cervical region of a 14 mm. cat embryo 
(series 222, slide VII, section 26), X 150. 

11 Jugular lymph sac. 

25 Internal jugular vein. 

27 External jugular vein. 

27' External jugular lymphatics. 



riGURE 10 
. Ill Same, slide VIII, section 4. 

11 Jugular lymph sac. 

25 Internal jugular vein. 

27 External jugular vein. 

27' External jugular lymphatics. 



I 



FIGURE 17 

17 Transverse section of upper thoracic region of 14 mm. embryo (series 37, 
slide XIII, section 12), X 150. 

1 Sympathetic nerve. 

3 Frecardinal or precava, resp. azygos of right side. 

6 Frecardinal or precava, resp. azygos of left side. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 
22 Vagus. 

53 Precaval lymphatics. 



FIGURES 18 AXD 19 

18 Transverse section of middle thoracic region in a 17 mm. cat embryo (series 
258, slide XVIII, section 9), X 225. 

19 Transverse section through mid-thoracic region of a 19 mm. cat embryo 
(series 253, slide XXIV, section 9), X 225. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos. 

4 Atrophying embryonal vein. 

5 Extraintimal or perivenous l>Tnphatic space. 

6 Left azygos. 

7 Aorta. 

15 Interazygos venous ple.xus. 

36 Azygos segment of thoracic duct. 



FIGURE 20 

20 Transverse section of upper abdominal region of a 17 mm. cat embryo, showing developing components of ascending Imnbar l3anphatic trunks and of mesenteric sac in relation to embryonic veins in the root of the dorsal mesentery and their 
relation to the cardinal collateral venous channels (series 258, slide XXIII, section 

•M), X 75. 

1 Sympathetic nerve. 

7 Aorta. 

51 Mesenteric lymphatics. 

58 Ureters. 

61 Iliac vessels. 

62 End gut. 

63 Ventral division of cloaca (urinary bladder). 

64 Wolffian ducts. 

66 Umbilical arteries. 

67 Right postcardinal vein. 

68 Left postcardinal vein. 

74 Cardinal collateral veins. 

75 Ascending lumbar hmphatic trunks. 



FIGURE 21 
21 Same section, X 150. 

7 Aorta. 

51 Mesenteric lymphatics. 

58 Ureters. 

67 Right postcardinal vein. 

68 Left postcardinal vein. 

74 Cardinal collateral veins. 

75 Ascending lumbar lymphatic trunks. 



FIGURE322 
22 Same, section 33. 

1 Sympathetic nerve. 

7 Aorta. 

51 Mesenteric lymphatics. 

68 Ureters; 

67 Right postcardinal vein. 

68 Left postcardinal vein. 

74 Cardinal collateral veins. 

75 Ascending lumbar lymphatic trunks. 



FRJURES 23 AND 24 



23 Same, section 32. 

24 Same, section 31. 

7 Aorta. 

61 Mesenteric lymphatics. 

67 Right postcardinal vein. 

68 Left postcardinal vein. 

74 Cardinal collateral veins. 

75 A.«<cending lumbar lymphatic trunks* 



25 Transverse section of posterior end of a 2() mm. cat eml)ryo (series 241, 
sli(ie XXX, section 4), X 75 — showing extraintimal replacement of left supra cardinal vein (59) by ascending lumbar relroaortic lymphatic channel (76). 

1 Sympathetic nerve. 

7 Aorta. 

58 Ureters. 

59 Left supracardinal vein. 

60 Right supracardinal vein. 

62 End gut. 

63 Ventral division of cloaca (urinary bladder). 

64 Wolffian ducts. 

65 Metanephros. 

66 Umbilical arteries. 

67 Right post cardinal vein. 
6S Left postcardinal vein. 

76 Hetroaortic supracardinal lyin])hatic trunks. 



FKJUUE 26 
26 Same, section 14, X 150. 

1 Sympathetic nerve. 

58 Ureters. . 

59 Left supracardinal vein. 

60 Right supracardinal vein. 

67 Right postcardinal vein. 

68 Left postcardinal vein. 

75 Ascending lumbar lymphatic trunks. 

76 Retroaortic supracardinal lymphatic trunks. 



FIGURE 27 



27 Reconstruction of anterior vascular complex in an IS mm. cat embrj^o 
(serie»< 88), X oO. Ventral view. 



FIGUUK 28 
28 Same, lateral view of left side. 



56 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

it increasingly turns to the left and continues to develop cephalad 
along the ventral surface of the inter-azygos plexus, by extraintimal replacement of elements belonging to the latter. (Compare the series of six reconstructions shown in figs. 188, 189, 
190, 191, 192, 193.) 

The details of the adult organization of the thoracic ducts, and 
the genesis of the observed adult variations on the basis of the 
development of the embryonic channels, will be considered subsequently (Part V). The present conmiunication is confined to 
the consideration of the development of the preazygos and 
azygos segments of the ducts. The thoracic ducts develop in cat 
embryos between 11 and 16 mm. crown rump measure. In the 
16 mm. embryo, McClure ^'•'' states that they ^4or the first 
time make their appearance as definite, continuous lymph channels, which are disconnected from the venous system, except 
through the mediation of the jugular lymph sacs.'^ This is the 
case in the majority of 16 mm. embryos, but in a number of 15, 
15 5 and 16 mm. series in my collection the final union of the 
individual segments has not yet taken place. It is possible, by 
combining a large number of observations on numerous embryos 
of the same length, to establish an average developmental condition of the thoracic ducts for each stage in embryos between 12 
mm. and 17 mm. crown-rump measure. Individual embryos 
will, however, show marked diflfereoces in development, and 
many departures from the standard plan are encountered. 
The same conditions obtain here which McClure and I found in 
our study of the development of the jugular lymph sacs. Some 
embryos show, for their length, unusually advanced thoracic 
duct development in certain areas, while in other parts this 
development is relatively retarded and more primitive. In other 
series the entire region of thoracic duct development appears 
more uniformly ahead of the average condition, normally encountered in embryos of this period. Finally, in a third group, 
the appearance of the typical lymphatic development seems to 
be delayed until a later stage than is normally the case. But in 
spite of these individual differences, a uniform and consistent 
ground plan of thoracic duct development can be demonstrated, to 



DEVELOPMENT OF THE THORACIC DUCT 57 

which the majority of embryos conform and into which even the 
aberrant types fit. As a matter of fact, the regularity with which 
the thoracic duct anlages first appear in the majority of the 
individuals of the proper stage, and the uniform and constant 
character of the resulting histological pictures, is one of the most 
striking and significant features of the entire process. Prior to 
the 11 mm. stage no definite anlage of the anterior segments of 
the future ducts is observable. 

I believe that the adult thoracic ducts of the cat are developed 
by fusion of three distinct and separate regional segments. Each 
of these segments is in turn formed by confluence of a number of 
originally discrete and independent anlages, which develop independently of the venous system as extra-intimal or perivenous 
mesenchymal spaces in the sense previously defined. ^*' '» -'• 
*^' These spaces are applied to, or surround, the walls of 
the embryonic veins of the lower cervical and of the dorsal 
mediastinal region. The three main divisions, thus developed 
independently of the venous system, unite with each other to 
form the channels of the left and right thoracic ducts, and these 
usually gain their point of entrance into the systemic veins by 
uniting with a process of the jugular lymph sacs ("thoracic duct 
approach") derived from their dorsal aspect, just cephalad to 
the common jugular approach. Exceptionally the main (left) 
thoracic duct, by combining with the ventral mediastinal trunk 
presently to be described, unites (fig. 98) with the ventral process 
of the "subclavian approach,'' prolonged from the jugular lymph 
sac over the ventral surface of the jugulo-subclavian confluence, 
and thus establishes its connection with the venous system (cf. 
pp. 84 89, figs. 89 to 99). 

The ontogenetic history of the ducts may therefore (fig. 29) 
be considered under four headings, viz. : 

1. The THORACIC duct approach of the jugular lymph sac, 
forming the terminal of the adult duct on each side (fig. 29, 1, blue) . 

2. The preaztgos segment (fig. 29, II). This includes two 
distinct and separate channels: 

A. The bronchO'Tnediastinal or ventral mediastinal lymphatic 
trunk (fig. 29, 37, green) , which drains the ventral mediastinum 



58 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

cephalad of the pericardium, viz., the pericardial, tracheal, 
bronchial, lateral oesophageal, and thymic areas. 

This lymphatic channel, associated with the embryonic venous 
plexuses of the pretracheal region, the pulmonary vessels and 
the vagi, develops through confluence of a large number of separate and independent extra-intimal lymphatic spaces following 
and surrounding the embryonic venous plexuses of the ventral 
mediastinum. The chain formed by these spaces eventually 
unites with the similar chain forming the anlages of the preazygos 
segment of the thoracic duct. 

B. The preazygos segment of the main thoracic duct (fig. 29, 55, 
brown). This portion of the main duct extends from the point 
of its entrance into the jugular lymph sac, through the thoracic 
duct approach of the latter, caudad to its intersection with the 
dorsal surface of the aortic arch. 

In the adult animal this segment forms the relatively long portion which ascends cephalo-sinistrad from the point where the 
duct parts company with the right azygos vein, to its junction 
with the jugular lymph sac, under cover of the aortic arch, and 
the vertical portion of the left subclavian artery, dorsal to the 
vertebral vein and to the left innominate confluence. In this 
part of its course the thoracic duct frequently receives the lymphatic return from the ventral mediastinum through channels 
which unite it to the ventral mediastinal trunk as just defined. 
The preazygos segment of the main duct is again formed in the 
embryo by confluence of independent mesenchymal spaces 
around and along the prevertebral and dorsal mediastinal venous 
plexuses of the embryo. 

3. The azygos segment (fig. 29, III, 36, yellow) comprises 
the portions of the thoracic ducts caudal to the level of the aortic 
arch. It develops, again independently, as the result of fusion 
of a number of extraintimal mesenchymal spaces closely applied 
to the ventral surface of the azygos veins, or of their ventromedial tributaries, or surrounding the latter. 

4. The post- azygos segment (fig. 29, IV, 52, green), through 
which the thoracic ducts establish their connection with the 
Receptaculum and the system of the abdominal lymphatics. 



DEVELOPMENT OF THE THORACIC DUCT 59 

Inasmuch as the development of this segment of both ducts 
is intimately connected with that of the principal abdominal 
lymphatic channels, its consideration will be included in that of 
the latter system (Part III). The present communication deals 
only with the first three segments above enumerated. 

Fig. 29 shows in a color schema the genetic composition of the 
thoracic ducts according to the segments just outlined, and their 
relation to the embryonic venous system. 

In proceeding caudo-cephalad the post-azygos portion (IV) 
develops in the larger right segment (52) by replacement of the 
caudal part of the ventro-medial tributary plexus of the right 
azygos vein. 

The smaller channel of the left side replaces the caudal part of 
the left azygos vein. In the azygos area (III) the left channel 
follows, as a much reduced left thoracic duct, the prevertebral 
portion of the left azygos vein. The larger right lymphatic 
channel {36), gradually inclining cephalo-sinistrad, develops 
along the ventral aspect of the inter-azygos cross-anastomosis 
and unites with the left duct eventually in a close plexiform interlacement perforated by the intersegmental arteries, which continues cephalad to near the level of the aortic arch. Here the 
plexus condenses into two more or less well defined channels 
which turn up to the right and left into the preazygos segment 
(II). The smaller right channel follows, cephalad of the right 
azygos terminal, the dorso-medial aspect of the right precaval, 
innominate and common jugular veins, developing by confluence 
of extraintimal spaces along the course of these vessels (ef . reconstruction of series 88, figs. 27 and 28), and forms the cephalic 
end of the reduced right thoracic duct of the adult. It terminates 
by joining the thoracic duct approach (12) of the right jugular 
lymph sac. The left and larger trunk replaces the extra-pericardial portion of the left precava, and ascends dorsal to the left 
innominate confluence to its junction with the thoracic duct 
approach {12) of the left jugular lymph sac. 37 in fig. 29 indicates* the broncho-mediastinal trunk in one of its commonly 
encountered types, joining caudally the preazygos portion of the 
thoracic duct (35), and terminating cephalad in the ventral 



60 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

process of the subclavian approach (14) of the jugular lymph sac, 
m company with the mam lymphatic channels retummg from 
the anterior extremity. 

1. THE THORACIC DUCT APPROACH OF THE JUGULAR LYMPH SACS 

(FIG. 29, 12) 

This Structure is an integral part of the jugular lymph sacs 
and forms in the adult animal the portal of entry of the thoracic 
ducts into the lymph sacs, and through them into the systemic 
veins. McClure, in the paper quoted ^^^^' has described its 
general formation and relation to the jugular lymph sac and has 
given an excellent illustration of its appearance in the dorsal 
view of a reconstruction of a 14 mm. cat embryo. I have here 
defined it as the "thoracic duct approach" of the sacs, in conformity with the nomenclature which McClure and I adopted 
in describing ^^s, 27; n^^ development of those portions of the 
jugular sac which, forming the "jugular" and "subclavian" 
"approaches," project as blind processes from the caudal end of 
the sac, and are destined to effect subsequently the permanent 
lymphatico-venous connections at either the common jugular, 
or the jugulo-subclavian confluence, or at both of these venous angles. The term, as here used in describing the similar process of 
the sac which is to establish definite connections with the thoracic duct, is intended to emphasize the fact that the ''thoracic 
approach" of the lymph sac is, like the rest of the structure from 
which it proceeds, verums in origin, while the thoracic ducts proper, 
with which it secondarily unites, are not derived from the veins, 
but are, from their beginning, independent of the bloodrvascular 
channels, and develop by confluence of independent extra- or perivenoiLs mesenchymal spaces. 

This fundamental difference in origin is shared, m my ophiion, 
by all the other main systemic lymphatics which, in addition to 
the thoracic ducts, enter the jugular sacs as the subclavian, external jugular, cephalic and internal jugular lymphatics through 
the processes which the sac sends to meet them. 

The thoracic duct approach of the earlier embryos arises as a 
short, blunt, curved, conical process from the dorso-medial aspect 



DEVELOPMENT OF THE THORACIC DUCT 61 

of the sac, a short distance cephalad of the jugular approach and 
of the common jugular venous confluence. 

It extends meso-caudad across the dorso-lateral and dorsal 
aspects of the mtemal and common jugular veins between them 
and the thyro-cervical artery, towards the vagus-sympathetic 
strand, dipping ventro-mesad between the main vein and the 
nerves and ending blindly in this situation. 

The process makes its first distinct appearance, after the 
jugular sac has been fully established, in embryos of between 11 
mm. and 14 mm. crown-rump measure. 

It is noteworthy that individual embryos within these limits 
show considerable diflference in the degree of development of the 
process. In some it appears earlier, in others* a little later, so 
that in individual instances an embryo of slightly shorter measure 
may have the thoracic duct approach of the jugular lymph sac 
further developed than one which exceeds the first in total length 
by the fraction of a millimeter. 

Thus one of the earUest distinct stages of the process is seen 
in a 14 nam. embryo (series 210, slide viii, sections 39-42, figs. 

30 to 33 inclusive). 

In this embryo, the thoracic duct approach appears as a short 
blunt process which projects dorso-mesad from the caudal end 
of the left jugular lymph sac, a short distance cephalad of the 
common jugular confluence. Sections 39, 40 and 41 (figs. 30, 

31 and 32, 12) show the earliest stage in the development of this 
process. In them the area dorsal to the main vein, between the 
sympathetic nerve and the jugular lymph sac, is occupied, in 
the direction meso-laterad, by the sympathetic nerve (/), the 
termination of the large dorso-meJial venous tributary (left 
sup. intercostal vein) (/6), the thyro-cervical artery {S4), and, 
laterad to this, by the blind terminal portion of the thoracic 
duct approach (/^), derived from the dorso-medial aspect of the 
jugular lymph sac (//). In this embryo the process of the sac 
ends blindly laterad to the thyro-cervical arter>^ (figs. 33, 34, ^4). 
It has not yet extended meso-caudad across the dorsal surface of 
the main vein toward the interval between the thyro-cervical 
artery and the sympathetic nerve. The thyro-cervical artery 



62 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

(24) lies at a little distance directly dorsad of the internal jugular 
vein. The dorso-medial angle of the main vein is related to a 
large compound medial venous tributary, draining the dorsomedial (prevertebral), (17) and the dorsal somatic areas (16). 
This compound vessel is the anlage of the future superior intercostal vein. In fig. 33 (section 42) the common trunk opens 
into the main vein just dorsal to the sympathetic nerve (1). 
In this section, the blunt medial extremity of the thoracic duct 
approach (12) is separated from the portion still connected with 
the jugular lymph sac, thus expressing the caudo-mesal curve 
of the entire process. It ends blindly in the following section, and 
does not reappear in the succeeding sections. The common jugular confluence occurs in section 44 of this slide. 

We are dealing, therefore, with a short, blunt conical process 
of the left jugular lymph sac, which curves meso-caudad for two 
sections, and terminates blindly dorsal to the main vein. 

In another 14 nun. embryo (series 212) the thoracic duct approach is much more extensively developed and occupies sections 
11 to 26 of slide ix. Selected sections of this series are shown 
hi figs. 34 to 42 inclusive. 

Fig. 34 (series 212, slide ix, sec. 14) shows part of the caudal 
end of the left jugular lymph sac (11) with the thoracic duct 
approach (12) arising from its medial aspect and extending mesad 
across the dorsal surface of the internal jugular vein (25). On 
the mesal aspect of the vein are seen the sympathetic (1) and 
the vagus (22). 

The large common trunk formed by the union of the dorsal 
somatic and prevertebral venous tributaries {16, 17) lies dorsomedial to the main jugular channel. It joins the latter, as left 
superior intercostal vein, {16, 46f) in section 26 of this slide 
(fig. 41). On the lateral aspect of this vessel is the ascending 
dorsal branch of the thyro-cervical artery {24). 

The six succeeding figures (35 to 40 inclusive) are cut down so 
as to only show the dorsal circumference of the internal jugular 
vein and the superincumbent thoracic duct approach of the 
jugular lymph sac. 

In fig. 35 (section 15) the approach has extended further mesad 



DEVELOPMENT OF THE THORACIC DUCT 63 

across the main vein. In fig. 36 (section 16) a blind terminal 
protrusion (12) separates from the main lumen of the sac (H), 
indicating the frequent bifid character of the thoracic duct approach. The succeeding sections (18 and 20, figs. 37 and 38) 
hence show an apparent recession of the entire process. In section 22 (fig. 39) the approach has again extended mesad toward 
the thyro-cervical artery and the superior intercostal vein. In 
the succeeding section (fig. 40) the fundus of the process terminates 
for the second time in a blind pouch-like protrusion (12), In the 
following section (24, fig. 41) -the approach (12) again appears 
fully developed and in open connection with the main jugular 
lymph sac (//). It maintains the character in section 25, and 
in section 26 (fig. 42) the terminal of this second protrusion (12) 
ends blindly. It does not reappear in the succeeding sections. 

We are dealing here with an instance of very common occurrence, in which the thoracic duct approach of these earlier stages 
not only gives off a number of blind terminal diverticula, but in 
which the entire approach arises by two or three distinct and 
separate origins from the main jugular lymph sac. This character 
will again be discussed below (cf. p. 66). in connection with the 
interpretation of certain adult conditions, but the instance now 
under discussion shows the early type of this variation very clearly, 
so that in a graphic reconstruction the thoracic duct approach 
of this embryo would appear as in figure on page 64. 

This embryo therefore presents for its age an unusually long 
and well developed thoracic duct approach, with triple terminal 
pouches, extending through sixteen sections, while at the same 
time it remains throughout this extensive course in the early 
position, viz.: lateral to the thyro-cervical artery (24) and the 
conmion trunk of the dorsal and dorso-medial tributaries of the 
internal jugular vein (16, 17, 46). The approach has not as yet 
arched mesad into the neuro-venous recess, and is hence in 
marked contrast to the succeeding stages presently to be described. 

In a 13.5 mm. embryo, series 189, the development of the thoracic duct approach has gone much further, although the embryo, 
a litter mate of series 210, measures half a millimeter less. 

The thoracic duct approach of the left jugular lymph sac 



64 



DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 



occupies sections 10 to 23 of slide vii in this embryo, and is 
shown in the dorsal view of the reconstruction, fig. 89, to which 
the individual sections following are referred for orientation. 

The process arises in the usual situation from the dorso-medial 
aspect of the left jugular lymph sac and trends dorso-mesad 




Subclavian V. 



across the internal jugular vein (series 189, sUde vii, section 10, 
fig. 43). In reference to the level of the common jugular confluence, which occurs in slide vii, section 26, the thoracic duct 
approach in series 189 arises more anteriorly from the jugular 
lymph sac than in the preceding series 210. Its extent and course 



DEVELOPMENT OF THE THORACIC DUCT 65 

can be followed accurately in the successive sections shown in figs. 
43 to 55 inclusive (series 189, slide vii, sections 10 to 22 inclusive). 

In section 11 (fig. 44) the thoracic duct approach is separated 
by a thin endothelial partition from the lumen of the main jugular 
lymph sac, which it rejoins in the following section (section 12, 
fig. 45), only to again separate in the next section (section 13, 
fig. 46). In the meanwhile, the thoracic duct approach has 
arched from the lateral to the medial side of the internal jugular 
vein {25), closely applied to its dorsal surface, between the same 
and the thyro-cervical artery (24) j and its blind terminal is 
beginning to bend ventro-mesad into the neuro-venous recess 
between the vagus-sympathetic strand {1 , 22) and the internal 
jugular vein {26). In the next three sections (sections 14, 15, 
16, figs. 47, 48 and 49) the thoracic duct approach becomes 
slightly dilated and diverticular (sections 15 and 16, figs. 48 and 
49), but remains detached from the jugular sac. In section 15 
(fig. 48) it appears subdivided, by endothelial partition, into two, 
and in section 16 (fig. 49) into three components. The protrusion which the common jugular confluence sends towards the 
jugular approach of the lymph sac and which forms the point 
of the subsequent invagination of the venous angle by the lymphatic tap, begins to appear in section 16 (fig. 49), and can be 
traced through the succeeding sections as a derivative of the lateral 
aspect of the main internal jugular vein, between it and the 
median surface of the jugular lymphatic sac. 

In the six following sections, 17 to 22 inclusive, (figs. 50 to 
55 inclusive) the proximal end of the process, connected with the 
sac, gradually recedes, while the blind distal end {12') conti. ues 
to develop in the ventro-medial direction between the main vein 
{25, in fig. 55) and the dorsal and dorso-medial venous tributaries 
{16 and 17, fig. 55), dipping ventrad and approaching the interval 
between the internal jugular vein {25) and the sympathetic 
nerve (i), the site of its subsequent junction with the independently developed perivenous lymphatics of the ventral mediastinal and dorsal prevertebral regions, which together constitute 
the anlages of this cephalic portion of the future thoracic duct, 
(cf. series 143, slides x and xi, figs. 172 to 183). The thoracic 
duct approach ends blindly in section 26 of slide vii. The 



66 DEVELOPMENT OF THE SYSTEiMIC LYMPHATIC VESSELS 

course and the relations to surrounding structures of the thoracic 
duct approach of this embryo are shov^rn in the dorsal view of 
the reconstruction (fig. 89), containing the 50 sections of slide 
vii in a magnification of 225 diameters. 

This view of the reconstruction presents from the lateral to 
the mesal border the following structures. 

1. Caudal end of left jugular lymph sac, with the jugular (13) 
and subclavian {14) approaches, between which passes the ventral 
branch of the thyro-cervical artery (24)
The fifth spinal nerve (54) penetrates the lymph sac, while 
the sixth nerve lies on its lateral aspect with the primitive ulnar 
veno-lymphatic arching over it to enter the lymph sac. 

2. The dorsal aspect of the internal jugular vein (25). 

3. The main trunk and branches of the thryo-cervical artery (24) . 

4. The left superior intercostal vein (46), with the dorsal {16) 
and dorso-medial or prevertebral {17) tributaries, enters thedorsomedial angle of the internal jugular vein between the thyrocervical artery {24) and 

5. the double strand of the vagus {22) and sympathetic (/) 
nerves. 

6. The thymus {21). 

7. The aortic arch (7), with the left carotid artery {23) and the 
origin of the innominate artery {45). 

The thoracic duct approach {12) arises by two branches from 
the dorso-medial aspect of the sac, turns caudo-mesad between 
the internal jugular vein and the ascending branch of the thyrocervical artery, in front of the left superior intercostal vein, and 
approaches the recess formed between the main vein and the 
bundle of the nerves. 

The reduplication of the origin of the thoracic duct approach 
from the jugular lymph sac present in this embryo is not unusual, 
and leads to the type of divided termination of the thoracic duct 
in the adult shown in fig. 56. The left jugular lymph sac (S) 
connects with the venous system at the common jugular angle 
{2) by a larger ventral and smaller dorsal jugular approach {18). 
It also taps at the jugulo-subclavian angle {19). The thoracic 
duct enters the dorsal aspect of the sac by a divided terminal, the 
lower branch connecting with the subclavian approach. 



DEVELOPMENT OF THE THORACIC DUCT 67 

Finally an intermediate condition is seen in another 14 mm. 
embryo, series 122, of which selected sections are appended, from 
slides ix and x (figs. 57 to 62). Section 21 of slide ix (fig. 57) 
is taken at the level where the jugular lymph sac has divided 
for the passage of the thyro-cervical artery (^34) into its two main 
terminal components, viz., the dorsally placed subclavian approach {14)j and the ventrally situated jugular approach (13), 
The latter appears in the interval between the internal jugular 
vein {25) and the jugulo-cephalic trunk (29), These veins are 
approaching each other to form the common jugular confluence 
(fig. 39, 26), at which point the jugular approach usually makes 
the secondar^-^ permanent lymphatico-venous tap. The thoracic 
duet approach {12) arises from the dorsal aspect of the jugular 
approach l.y a relatively narrow pedicle and then hooks, as an 
elongated and expanded curved pouch, ventro-mesad over the 
dorsal aspect of the internal jugular vein towards the neurovenous recess. 

In section 28 of the same slide (fig. 58) the internal jugular 
and jugulo-cephalic veins have met in the coimnon jugular confluence {26} which includes the jugular approach. Consequently 
the latter structure only appears in its ventral prolongation which 
is seen occupying the ventral angle of the conamon jugular junction (not labelled in fig. 58). 

The subclavian approach {14) has moved relatively nearer to 
the dorsal surface of the main vein channel. 

The blind terminal end of the thoracic duct approach {12) is 
seen dorsal to the common jugular vein, between a large dorsomedial tributary of the latter {16) mesally, and the thyro-cervical 
artery {24) laterally. Its pointed extremity is directed further 
ventro-mesad toward the interval between the sympathetic nerve 
(/) and the medial surface of the common jugular vein {26). 

In section 7 of slide x (fig. 59) the terminal of the thoracic 
duct approach {12) has relatively receded and lies in the narrow 
interval between thyro-cervical artery (24) and common jugular 
vein {26), 

In fig. 60 (section 9 of slide x) a large dorso-medial venous 
tributary {16, left superior intercostal vein) empties into the 



68 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

dorso-medial angle of the common jugular trunk. The thoracic 
duct approach {12), occupying the same relative position as in the 
preceding figure, lies between this tributary and the thyro-cervical artery, dorsal to the main vein. Section 12 of slide x (fig. 
61) shows the distal reduced end of the approach in this same 
situation. The subclavian approach of the jugular lymph sac 
(14) is reduced to a narrow longitudinal cleft on the dorso-lateral 
aspect of the main vein. This reduction is coincident with the 
derivation from the dorsal aspect of the subclavian approach of 
the primitive ulnar veno-lymphatic (31). This channel arches 
dorsad over the Vlth spinal nerve (30), and appears in this section in its typical relation to this nerve. Finally in the succeeding section, 13 of slide ix, (fig. 62), the thoracic duct approach 
ends blindly. The structures shown in the section dorsal to 
the common jugular trunk are now encountered in the following 
order: mesally the terminal of one of the branches of the dorsomedial venous plexus (16) ; next the thyro-cervical artery (24) ; 
then the Vlth segmental nerve (30), and, dorsal of this, the 
primitive ulnar veno-lymphatic (31), 

The series of sections of this embryo shown here are interesting not only in respect to the behavior of the thoracix; duct 
approach, but also in reference to the mutual relations of this 
structure and the terminals of the dorso-medial tributary venous 
plexus. These relations are to be discussed subsequently in considering, as whole, the evidence upon which some investigators 
have based their conception of direct venous origin of the lymphatic system by fusion of a number of separate elements detached from the main venous trunks (cf. infra p. 153.) 

The variable appearance of the thoracic duct approach in the 
younger stages is perhaps best illustrated by the exaggerated 
development presented in a 13 mm. embryo (series 92), in which 
the process occupies the last thirteen sections of slide x, and the 
first fourteen sections of slide ix. Selected microphotographs 
of this series are shown in figs. 63 to 78. The embryo presents 
the largest and most dilated thoracic duct approach of any in my 
collection. Fig. 63 gives a topographical view of the region 
involved. The succeeding sections are cut down and confined 



DEVELOPMENT OF THE THORACIC DUCT 69 

to the immediate neighborhood of the thoracic duct approach. 
Fig. 63 shows the sections of the internal jugular vein {25) and 
jugulo-cephalic trunk {29), approaching their point of union in 
the common jugular confluence. A large process of the jugular 
lymph sac {IS) extends, as the jugular approach, into the interval 
between the main veins. Along the mesal aspect of the internal 
jugular vein {25) are placed the sympathetic (i), the vagus {22), 
the left common carotid artery {23), and, further ventrad, the 
thymus {21 ) . The dorsal portion of the sac is about to form the 
subclavian approach {11, 14)
In fig. 64, the jugular approach {13) has entered more deeply 
into the narrowing interval between the internal jugular {26) 
and jugulo-cephalic trunks {29), and the sharply marked constriction between it and the remainder of the sac (subclavian 
approach, 14) foreshadows its coming separation from the latter. 
A protrusion of the dorso-medial angle of the jugular approach, 
adjacent to the internal jugular vein, indicates the beginning 
derivation of the thoracic duct approach {12). 

In the succeeding section (fig. 65) the jugular approach {IS) 
has separated from the subclavian approach {14) of the jugular 
lymph sac and thus cleared the path for the passage of the thyrocervical artery {24) between the two cardinal divisions of the 
lymph sac, whose caudal terminations are represented by the 
jugular and subclavian approaches. The origin of the thoracic 
duct approach {12) from the dorso-medial angle of the jugular 
approach -is now defined. 

In the succeeding section (fig. 66) the triple termination of the 
jugular lymph sac, in the subclavian (i^), jugular {IS) and thoracic duct approaches {12), is accomplished, and the latter is beginning to extend mesad across the dorsal surface of the internal 
jugular vein. The main thyro-cervical artery is approaching 
the junction with its secondary dorsal branches. 

In fig. 67 the jugular approach {IS) has divided into the intermediate part between the internal {25) and jugulo-cephalic {29) 
veins, which is to establish the tap at the common jugular angle, 
and a ventral process which extends from the tap caudad over 
the ventral surface of the common jugular angle and vein. 



70 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

The thoracic duct approach has enlarged, is partially subdivided 
(cf. p. 65, figs. 48 and 49, series 189) and its blind terminal 
extremity is reaching ventro-mesad into the angle between internal 
jugular vein and sympathetic (i). The thyro-cervical artery (£4) 
lies between the subclavian and thoracic duct approaches, dorsal 
to the jugulo-cephalic trunk (29). 

In fig. 68 the thoracic duct approach has further enlarged and 
is still subdivided into two compartments the terminal of which 
abuts directly against the sympathetic nerve. The jugular 
approach (13) communicates in this section with the internal 
jugular vein, while a narrower slit-like division continues further 
caudad toward the common jugular angle. 

In fig. 69 the internal (25) and jugulo-cephalic (29) trunks are 
only separated from each other by a narrow septum containing 
the lumeYi of the slit-like prolongation of the jugular approach. 
Both in this and in the preceding section the ventral process of 
the jugular approach lies in the angle between the two veins, 
closely applied to their ventral surface. 

The thoracic duct approach is a large sau.sage-shaped structure, 
curved over the dorsal surface of the internal jugular vein. The 
septum in its interior has disappeared and the process presents a 
clear lumen. 

In fig. 70 (slide ix, section 2), the confluence of internal jugular 
and jugulo-cephaUc trunks has taken place (26). The thoracic 
duct approach (12) has extended both ventro-mesad into an area 
of indifferently defined mesodermal spaces, mesad to the sympathetic nerve (1), and laterad- toward the subclavian approach 
of the jugular sac (14)j passing between common jugular vein 
(26) and thyro-cervical artery (24)
In section 5 of slide ix (fig. 71) the thoracic duct approach 
(12) appears as a long curved multilocular channel, which laterad 
reaches the subclavian approach of the jugular lymph sac, between 
the thryo-cervical arterj^ (24) and common jugular vein (26)j 
while its blind mesal extremity terminates just dorsal to the sympathetic-vagus strand. In the following section (fig. 72) the 
thoracic duct approach (12) connectswith the subclavian approach 
(14) of the jugular lymph sac affording an instance of the gene


DEVELOPMENT OF THE THORACIC DUCT 71 

sis of the reduplicated or multiple thoracic duct terminations occasionallj' encountered in the adult as above described (cf.p. GH, 
fig. 56, series 212, slide ix, figs. 34 to 42). 

In fig. 73 (series 92, slide ix, section 9) the subclavian approach 
[14) is much reduced, and lies along the lateral aspect of the common jugular vein (26). Its connection with the thoracic duct 
approach (12) is plainlj' visible, passing between the main vein 
(26) and the thyro-cervical arterj' (24)- Dorsal somatic and 
prevertebral venous tributaries (16), approaching the dorsomedial angle of the common jugular vein (26), intersect the course 
of the thoracic duct approach, and begin to divide the same into 
a medial and a lateral element. This division is completed in 
the following section (fig. 74) in which the united dorsal and prevertebral tributaries form a venous trunk of considerable size 
(16) which is approaching its confluence with the comimon jugular 
vein by passing between the lateral and medial components of 
the thoracic duct approach. In other words, the appearance of 
the thoracic duct approach in this and in the following sections 
is the expression of the ventro-mesal arched course of this structure 
across the fork or angle between the common jugular vein (26) and 
the terminal of its ventro-medial tributary plexus (16). The reconstructions shown in figs. 89, 90 and 91 indicate this topographical 
relationship clearly. The blind mesal end of the arched process 
(12) now lies mesal to the tributary vein (16) and dorsal to the 
sympathetic nerve (7). In the following section (section 11 of 
slide ix, fig. 75), the dorso-medial venous tributary (16) is elongated and close to the main vessel, while the reduced sections of 
the thoracic duct approach lie on either side of the same, as indicated by the forked leader (12), The subclavian approach (14)y 
still prominent and connected with the medial section of the 
thoracic duct approach in the preceding section 10 (fig. 74), 
appears now in section 11 reduced to a detached small blind end 
(not labelled in the figure), close to the lateral wall of the main 
vein and ventral to the thyro-cervical artery (24)- In the succeeding section 12 (fig. 76) the dorso-medial venous tributary 
(superior intercostal vein) enters the common jugular trunk. 
The lateral portion of the thoracic duct approach (not lal)elled 



72 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

in the figure) is seen in the deep recess between this entrance, 
the main vein {S6) and the thyro-cervical artery (24) . The mesal 
end of the thoracic duct approach terminates blindly in this 
section just dorsal to the sympathetic nerve (1). In section 13 
(fig. 77) the lateral terminal of the thoracic duct approach (IS) 
can still be clearly seen in the interval between the wide dorsal 
opening of the combined somatic and prevertebral (17) tributary 
stem into the main vein (26) and the thyro-cervical artery {S4) . 
It appears very much reduced in the same situation in section 
14 (fig. 78), and ends blindly in the following section. The last 
three sections of this series (figs, 76, 77 and 78) show the beginning of the jugulo-subclavian confluence. 

In the later stages the thoracic duct approach has extended 
further ventro-mesad into the recess between the common jugular 
vein and the sympathetic nerve, and in this situation it eventually 
makes its connection with the two independently developed lymphatic channels of the anterior mediastinal region, viz., the 
preazygos segment of the thoracic duct dorsally, and the bronchomediastinal trunk ventrally. The mode of this union is discussed below under a separate heading (cf. infra, p. 111). Figs. 
79 to 82 show transverse sections of the left side of the lower 
cervical region in a 15 mm. cat embryo (series 245, slide xi, 
sections 24 to 27, X 225), and fig. 90 gives the dorsal view of the 
reconstruction on the same scale of the thoracic duct approach 
and the related structures in the same embryo (slide xi, sections 
1-44). In fig. 79 (sUde xi, section 24) the terminal extremity 
of the thoracic duct approach (12) is seen between the common 
jugular vein {S6) and the sympathetic nerve (1), having reached 
this situation by extending ventro-mesad across the dorsal tributary 16 (left superior intercostal vein), between this vessel and 
the main venous trunk. 

The section is taken below the common jugular confluence, 
consequently the jugular approach is no longer seen, and the 
blind end of the thoracic duct approach appears isolated. The 
only other portion of the jugular lymph sac carried caudad to this 
level is the subclavian approach (14), seen on the lateral aspect 
of the main vein. The sequence of structures now successively 



DEVELOPMENT OF THE THOKACIC DUCT 73 

encountered along the mesal and dorsal aspects of the main common jugular vein (26) are the following, proceeding meso-laterad : 

1 . Thymus (21 ) , with sub- and suprathymic venous tributaries 
entering the main vein. 

2. Left common carotid artery (23), 

3. Vagus nerve (22). 

4. Sympathetic nerve (i). 

5. Thoracic duct approach (12), 

6. Dorsal somatic tributary of main vein (16). (Anlage of 
left superior intercostal vein). 

7. Thyro-cervical artery (24) 
8. Subclavian approach of jugular lymph sac (14), on the 
dorso-lateral aspect of the common jugular vein. 

This order and relationship is maintained uniformly and clearly 
in the three succeeding sections shown in f gs. 80, 81 and 82. 

In the last of these the dorsal venous tributary {16) enters the 
main common jugular channel. 

The sections can be easily followed and oriented by reference 
to the dorsal view of the reconstruction shown in fig. 90. The 
same is composed of the plates of all 44 sections of slideix of series 
245. In this embryo the thoracic duct approach has already 
established its definite and permanent connection with the independently developed channel of the preazygos segment of the 
thoracic duct {36, in fig. 90), as described in detail below (cf. 
p. 111). The point of this junction is indicated in the reconstruction by the narrowing of the two spindles 12 and 35 (thoracic 
duct approach and preazygos segment of thoracic duct) to form 
an isthmus situated just cephalad of the leader marked 16-46, 

The reconstruction includes the terminal of the jugular approach {13), with the origin from the same of the thoracic duct 
approach {12), and the entire subclavian approach {14) of the 
jugular lymph sac. The ventral division of the thyro cervical 
artery {24) passes forward between the jugular and subclavian 
approaches of the lymph sac, accompanied by a vein (not labelled 
in the figure) which is constantly found in this situation in the 
adult, draining from the prevertebral area into the common 
jugular trunk. 



74 DEVELOPMENT OP THE SYSTEMIC LYMPHATIC VESSELS 

The dorsal and dorso-medial venous tributary plexus has 
united into the stem of the left superior intercostal vein (16-46). 
The reconstruction shows well the caudo-mesal turn of the 
thoracic duct approach (12) in the fork between the main vein (26) 
and the superior intercostal (16-46), accompanied by the mesal 
branch of the thyro-cervical artery. The terminal of the thoracic duct approach (IZ) meets and unites with the preazygos 
segment of the thoracic duct (35) on the mesal shoulder of the 
superior intercostal vein terminal, between it and the sympathetic 
nerve (1). This is one of the two types of topographical relationship encountered (cf. infra pp. 75, 76). Further laterad follow 
the vagus (22) and the sympathetic strand (1), intersecting at an 
acute angle. Then the left common carotid artery (23) and the 
thymus (21) with the perithymic venous plexuses. 

Figs. 83 to 88 show the caudal end of the left jugular lymph 
sac and the thoracic duct approach in a selected series of sections 
from a 17 mm. cat embryo (series 142), all magnified 225 diameters, and fig. 91 gives the dorsal view of the reconstruction of 
this region from the same embryo. 

These preparations are introduced here for the purpose of 
illustrating, in comparison with the preceding series (245) the 
second type of relationship which the thoracic duct approach 
may bear to the combined vagus-sympathetic strand. 

Fig, 83 (series 142, sUde x, section 13) shows the transection 
of the caudal end of the left jugular lymph sac in the interval 
between the internal jugular (25) and jugulo-cephalic (29) veins 
which are approaching their confluence to form the common 
jugular trunk. 

The form of the jugular lymph sac already indicates its coming 
division into the three terminal '' approaches," the jugular approach (14), the subclavian approach (IS) and the thoracic duct 
approach (12). The latter covers the entire dorsal circumference 
of the internal jugular vein (25) and its termination points to the 
angular recess between the sympathetic (1) and vagus (22). 
Ventrad to the latter the field includes the thymus (21). The 
thyro-cervical artery is cut in several of its divisions, two of which 
are indicated by the forked leader 24


DEVELOPMENT OF THE THORACIC DUCT 75 

In fig. 84 (series 142, slide x, section 16), the subclavian approach (14) has separated from the jugular approach (13) and 
the thyro-cervical artery (24) is passing meso-laterad between 
these two divisions. The origin of the thoracic duct approach 

(12) from the dorso-medial circumference of the jugular approach 

(13) is well shown in the section. The concavity of the jugulocephalic arch is expressed by the two cross-sections labelled 29. 

In fig. 85 (series 142, slide x, section 8) the thoracic duct 
approach (12) has separated from the jugular approach (IS). 
The curve of the process, with the concavity directed mesocaudad, gives the two cross sections of its lumen included in the 
forked leader 12. The termination of the thoracic duct approach 
has still further invaded the recess between sympathetic (1) and 
vagus (22) and a slight interval has developed between the two 
nerves. 

The lateral circumference of the vagus (22) covers practically 
the entire mesal aspect of the internal jugular vein (25). 

In the following figure (fig. 86, series 142, slide x, section 20) 
the termination of the thoracic duct process (12) is seen slipping 
through the interval between sympathetic (1 ) dorsally and vagus 
(22) ventrally. Instead of lying therefore dorso-lateral to the 
sympathetic — as in the preceding series 245 — the end of the 
thoracic duct approach in the present instance passes mesad on 
the ventral aspect of this nerve, between the same and the vagus. 
This relationship is also seen in the two succeeding figures, 87 
and 88 (series 142, slide x, sections 22 and 24.) 

We are dealing therefore apparently with two potential paths 
which the blind terminal of the thoracic duct approach may take 
in its passage from the jugular lymph sac mesad beyond the vagussympathetic line to the upper mediastinal region, where it establishes eventually its secondary connections with the preazygos 
segment of the thoracic duct and with the broncho-mediastinal 
trunk. In one type (illustrated by the sections and reconstructions of series 245 (figs. 79 to 82, fig. 90) the process dips, after 
passing between the left superior intercostal and main jugular 
vein at an acute angle, caudad on the lateral side of the sympathetic strand (fig. 90). 



76 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

In the other type, illustrated by series 142 (figs. 83 to 88; fig. 
91) the thoracic duct approach, maintaining the identical relation 
to left superior intercostal and common jugular veins, gains the 
ventro-medial aspect of the sympathetic cord, by passing obliquely between the same and the vagus. 

In schematic cross section these two conditions may be illustrated by the accompanying text figures: 



In regard to the remaining structures fig. 87 (series 142, slide 
X, section 22) shows, by comparison with the preceding figure 
86, the tap of the jugular approach into the internal jugular vein 
(25) just above the confluence with the jugulo-cephalic trunk 
(29), and the prolongation of its ventral process {IS) over the 
ventral aspect of the common jugular angle. Fig. 88 (series 142, 
slide X, section 24) shows the confluence of the internal jugular 
(S5) and jugulo-cephalic (^9) veins fully established, and gives 
a very clear picture of the relation which the ventral prolongation 
(IS) from the jugular approach of the lymph sac bears to the 
common jugular angle. In both figs. 87 and 88 the dorsal venous 
tributary (sup. intercostal vein anlage) is indicated by the 
leader 16. It enters the main vein in section 3 of the following 
slide (xi). Fig. 91 gives the dorsal view of the reconstruction 
of the vascular and nervous structures of the left side in slides 



DEVELOPMENT OF THE THORACIC DUCT 77 

X and xi of this embryo, carried caudad to the level of the vertebral vessels Wl, 4^). Comparison with fig. 90 will show the 
correspondence of the two preparations in all essential points and 
will accentuate the above described difference in the course of 
the thoracic duct approach (12) and tjie preazygos segment of 
the thoracic duct (35) in relation to the vagus-sympathetic strand. 

It is readily seen, in comparing the reconstructions of the two 
older stages just described (figs. 90 and 91) with that of the 
earlier embryo shown in fig. 89, that the latter, in the construction 
of the terminal of its thoracic duct approach, combines potentially the ability of developing into either one of the two more 
advanced conditions just described. The process which the 
thoracic duct approach turns nearly horizontally mesad into the 
interval between vagus and sympathetic is present in all three 
reconstructions. In many embryos, as will appear presently in 
describing the critical stages in detail, the thoracic duct approach 
appears to make its connection with the independently developed 
anlages of the preazygos portion of the thoracic duct in this situation, and continued development will lead to the condition seen in 
series 142 (fig. 91). If, on the other hand, the caudal extremity 
of the thoracic duct approach of the 13.5 mm. embryo (fig. 89) 
joins the independently developed lymphatic anlages at the root 
of the left superior intercostal vein and along the common jugular 
lateral to the sympathetic line, the resulting relation will be as seen 
in series 245 (fig. 90). 

These observations are further supported by comparison of the 
preparations just described with the corresponding portions of 
the two reconstructions shown in figs. 170 and 171. 

Fig. 170 (series 218) shows the stage in a 15 nam. embryo just 
prior to the junction of the thoracic duct approach with the independently formed preazygos segment of the thoracic duct (35). 
The latter is in its greater part already a distinct and considerable 
segment of the future continuous duct channel. Between its 
blind cephalic extremity and the blind caudal end of the thoracic 
dUct approach (12) are a number of scattered and still separate 
lymphatic anlages along the common jugular and innominate 
veins on each side of the sympathetic line. By continued exten


78 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC* VESSELS 

sion of these as yet isolated lymphatic anlages the still lacking 
intermediate bondpiece will be produced, which, by union of its 
cephaUc extremity with the thoracic duct approach of the jugular 
lymph sac and junction of its caudal end with the cephali? termnal 
of the preazygos segment of the thoracic duct {35), will produce 
the continuous and uninterrupted lymph channel of the succeeding stage (se.ies 143, 15.5 mm, embryo, fig. 171). A study of the 
reconstruction of series 218 makes it evident that the opportunity 
still exists of developing this final junction either on the dorsolateral or ventro-medial side of the sympathetic cord, for the 
lymphatic anlages exist in both situations. The end of the 
thoracic duct approach of this embryo rides with a well marked 
lateral and medial prolongation in the fork formed by the entrance 
of the left superior intercostal vein (16-46) into the common 
jugular. The lateral process, carrying the leader 12 in the figure, 
is in position to join the line of separate lymphatic anlages extending caudad on the lateral side of the sympathetic, and a prominent 
cephalic process of the already established segment of the preazygos lymph channel extends cephalo-laterad across the dorsal 
surface of the nerve, as if to meet the lymphatic line just described. 
If development had proceeded along this line in this embr^^o, the 
condition seen in series 245 might have resulted, with the modification of swinging the thoracic duct approach to the lateral 
instead of to the medial side of the left superior intercostal vein, 
but carrying the thoracic duct along the dorso-lateral aspect 
of the sympathetic nerve. In this case the large separate lymphatic anlage labelled 35' in fig. 170 would take an important 
share in building up the resulting lymph channel. On the other 
hand, the definite connection with the preazygos segment of the 
thoracic duct might have been established through the ventromedial terminal prolongation of the thoracic duct approach. A 
piece of the sympathetic nerve has been removed in the reconstruction in order to show the position of this structure, in the 
interval between sympathetic nerve (1) and vagus (22), The 
long slender prolongation extending forward between vagus (22) 
and common carotid arter\^ (23) is the path of junction for the 
ventral or broncho-mediastinal lymphatic trunk. I am under 



DEVELOPMENT OP THE THORACIC DUCT 79 

the Strong impression that the observed variations in the relation 
of the embryonic thoracic duct approach to the sympathetic 
nerve hinge largely for their production upon the share which 
the broncho-mediastinal duct is to take in individual cases in 
the establishment of the preazygos segment of the thoracic duct 
channel. (Compare relations of 35 and ^7 in the schematic 
cross sections shown above in the text figures.) 

If now this ventro-medial end piece of the thoracic duct 
approach had effected its junction with the preazygos segment of 
the thoracic duct along the line of the lymphatic anlages on the 
medial side of the sympathetic and in the interval between this 
strand and the vagus, then the individual condition already described in series 142 (fig. 91) would have resulted. 

This same topographical relationship of sympathetic nerve and 
lymph channel is also seen in the 15.5 mm. embryo, series 143, 
shown in reconstruction from the right side in Fig. 171. The 
thoracic duct approach (12) intersects the sympathetic nerve {1) 
on its ventro-medial aspect at an acute angle to establish its connection with the cephalic end of the preazygos segment of the 
thoracic duct (36). This t>T)e appears the prevalent one in the 
embryos in my collection. 

I am strongly inclined, on the evidence of the embrj^os of my 
collection, to regard the development of the thoracic duct approach 
of the jugular lymph sac as occupying three distinct chronological 
stages : 

1. Early stage. Embryos of 13-13.5 mm. 

Series 92 — 13. nam. 

Series 189 — 13.5 mm. 
In this period the thoracic duct approach appears large, at 
times multilocular, and shares the redundancy and capacious 
lumen which characterizes the entire jugular h^mph sac in the 
earlier genetic period. 

2. Intermediate stage. Embryos of 14 mm. 

Series 210 — 14 mm. 
Series 212 — 14 mm. 
Series 122 — 14 mm. 
The sac, as a whole, and the thoracic duct approach in })articu


80 DEVELOPMENT OT THE SYSTEMIC LYMPHATIC VESSELS 

lar, condenses and becomes more clearly defined against the surrounding mesoderm. The multilocular character due to remnants of the capillary walls in the interior, disappears and the 
approach obtains a clear and clean-cut lumen. The entire structure appears to contract somewhat on itself and develops more 
distinct walls. The recession, during which the thoracic duct 
approach occupies a relatively smaller territory is succeeded by 
3. Final stage. Embryos of 15-17 mm. 

Series 245 — 15 mm. 

Series 218 — 15 mm. 

Series 143 — 15.5 mm. 

Series 142—17 mm. 
In this period the sac, through its digitate processes, establishes 
the definite connections with the independently formed systemic 
extraintimal lymphatic channels. Specifically the thoracic d uct 
approach of the sac unites secondarily with the preazygos segment of the thoracic duct and with the broncho-mediastinal 
lymphatic trunk. 

While I do not insist on the above outlined details in the 
chronological order of development of the thoracic duct approach, 
the embryos of my collection certainly tend to support the view 
expressed. Thus the 13 mm. embryo (series 92) offers the 
highest degree of expansion of the thoracic duct approach. The 
structure recedes and diminishes somewhat in extent in the 
13.5 mm. stage (series 189), appears uniformly further reduced 
and shortened in the 14 mm. embryos (series 210, 212, 122), and 
finally, from the 15 and 15.5 mm. stages on, makes its definite 
connections with the preformed independently developed channels of the thoracic and broncho-mediastinal ducts. 

In this entire genetic process there is not the slightest indication of an extension of lymphatic trunks from the jugular sac or 
from its thoracic duct approach toward the periphery. There 
is absolutely no suggestion of so-called ^'budding" or ^* sprouting,'' or of any other form of centrifugal extension of lymphatic 
vessels. On the contrary, the sac as a whole, and the processes 
therewith connected, recede actually for a time, and only then 
establish a secondary junction with the independently developed 



DEVELOPMENT OF THE THORACIC DUCT 81 

general systemic lymphatic channels. These have in the meanwhile formed along and around the temporarj"^ embryonic veins, 
as the result of the confluence of large numbers of extraintimal 
perivenous spaces in the sense previously defined in detail. 
Then- line of further growth, extension and union with each other 
is altogether centripetal^ from the outlying regions toward the 
jugular lymph sacs, and theh- union with the latter 's processes 
is the last and final step in the definite organization of the lymphatic sj^stem. 



PART II, PLATES 

FIGURES 29 TO 91 



FIGTRi: 2? 



TSf Cc4or B^ita^aL. Otfviz^ ilie 5 cmr enwiir seexDesic oi ^ht ikorMor tens 1. 
IL IIL n~ IK lirt- ca^L &ad l2«Lr rrdkiiocis :<:< ihs ^s^hrpomal tcebs. ike 



Z" PreeferdzcdJ w pmaT% oc rii^t fade. 

6 PmeardixuJ ^r prcicjiXft <iif Ic^i fSie 

G' Left Axxroe i:^nxL. Thamnc ponSooL 

7 AoTLfc. 

11 iufolkr hnz-p^ fiii^
12 infnliLr }tz4^ «{fc.ei. iboni^i? -ii;^ &3?pnMch. 

13 iiariilair IriLp&i ia«r- jcrcl^ jippnoc^ 

14 iiafolu' IjrrT^i fibc sobc-l^iiiaa 3ipf»nac^ 

•26 C^ecLfOC jucnW T«d=L. 

33 ScbfliTitiJ »rt«rT 

3T ST^irlAT-ikn t*-:^. 

35 TbfWirif^ d-r:- prekxygos 

37 Br*:-c*cii«>-c>'»'iikftsrjJ c-n. 

£ Pon^jj^o* M«cL«i-. of :LorA^-> i-n. 



FIGUHKS 3<) AND 31 

30 'VriiiiHXfrHO. Hortion throiif|;h left hu\c of lower cervical region in a 14 iiitn. rat 
embryo («ericH 210, sliile VI 11. section 39>, X 225. 

31 Same, flection 40. 

1 Sympathetic nerve. 

1 1 Jugular lymph sac. 

12 JuKular lymph sac, thoracic duct approach. 

16 DorHo-medial somatic venous tributaries. 

17 Pn? vertebral venous plexus. 

18 Peritracheal venous plexus. 

19 Suprathymic venous plexus. 

20 Subthymic venous plexus. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 

25 Internal jugular vein. 



FIGURES 32, 33 AND 34 

32 Same, section 41. 

33 Same, section 42. 

34 Transverse section through left side of lower cervical region in a 14 nun. rat 
embryo (series 212. slide IX. section 24), X 200. 

1 Sympathetic nerve. 

8 Oesophagus. 

11 Jugular lymph sac. 

12 Jugular lymph sac, thoracic duct approach. 

16 Dorso-medial somatic venous tributaries. 

17 Prevertebral venous plexus. 

18 Peritracheal venous plexus. 
22 Vagus. 

24 Th3rrocervical artery. 
2o Internal jugular vein. 



FIGURES 35 TO 41 

35 Sainc, section 15. 

36 Same, section 16. 

37 Same, section 17. 

38 Same, section 20. 

39 Same, section 22. 

40 Same, section 23. 

41 Same. secti(m 24. 

1 Sympathetic nerve. 

11 Jugular lymph sac. 

12 Jugular l^Mnph sac, thoracic duct approach. 
16 Dorso-metlial somatic venous tributaries. 
22 Vagus. 

24 Thyrocervical artery. 

25 Internal jugular vein. 

46 Left superior intercostal vein. 



FIGUKKS 42 AND 4.S 

42 Same, section 26. 

43 Transverse section through left side of lower cervical region of a 13.5 mm 
cat embryo (series 189, slide VII, section 10), X 150. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

11 Jugular lymph sac. 

12 Jugular lymph sac, thoracic duct approach. 

16 Dorso-medial somatic venous tributaries. 

17 Prevertebral venous plexus. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 

25 Internal jugular vein. 

46 Left superior intercostal vein. 



FIGURES 44 TO 49 

44 Same, section 11. 

45 Same, section 12. 

46 Same, section 13 

47 Same, section l4. 

48 Same, section 15. 

49 Same, section 16. 

1 Sympathetic nerve. 

8 Oesophagus 

9 Trachea. 

11 Jugular lymph sac. 

12 Jugular lymph sac, thoracic duct approach. 

16 Dorso-medial somatic venous tributaries. 

17 Prevertebral venous plexus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 

25 Internal jugular vein. 
29 Jugulo-subclavian tnmk 



FICJUJiKS 50 TO 5o 

50 8ainc, section 17. 

51 Same, section 18. 
62 Same, section 19. 

53 Same, section 20. 

54 Same, section 21. 

55 Same, section 22. 

1 Sympathetic ner\e. 

S Oesophagus. 

11 Jugular lymph sac. 

12 Jugular lymph sac, thoracic duct approacli. 
IG Dorso-medial somatic venous tributaries. 
17 Prevertebral venous plexus. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 

25 Internal jugidar vein. 

21» Jugulo-subclavian trunk. 



FIGURE 56 

56 Dissection of left cervical region of adult cat, showing reduplication (»f 
thoracic duct approach of left jugular lymph sac (Adult No. H3). 

1 External jugular vein and lymphatics. 

2 Common jugular vein. 

3 Jugular lymph sac. 
5 Subclavian vein. 

9 Thyrocervical artery. 

1 1 Vertebral vein. 

13 Left subclavian artery. 

18 Jugular approach and tap. 

10 Subclavian approach and tap. 

20 Innom inate artery . 

24 Vena cava superior. 

25 Left carotid artery. 

26 Aorta. 



FIGURES 57 AND 58 

57 Transverse section through left lower cervical region of a 14 mm. cat embryo 
(series 122, slide IX, section 21) , X 150. 

58 Same, section 28. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

12 Jugular lymph sac, thoracic duct approach. 

13 Jugular lymph sac, jugular approach. 

14 Jugular l3nmph sac, subclavian approach. 
16 Dorso-medial somatic venous tributaries. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 

25 Internal jugular vein. 

26 Common jugular vein. 
29 Jugulo-subclavian trunk« 



\ 



FIGURES 59, 60 AND 61 

59 Same, slide X, section 7. 

60 Same, section 9. 

61 Same, section 12. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

12 Jugular lymph sac, thoracic duct approach. 

14 Jugular lymph sac, subclavian approach. 

16 Dorso-medial somatic venous tributaries. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 
26 Common jugular vein. 

30 Sixth spinal nerve. 

31 Primitive ulnar veno-ljrmphatic. 



FIGURES 62 AND 63 

62 Same, section 13. 

63 Transverse section of left lower cervical region in a 13 mm. cat embryo 
(series 92, slide X, section 27), X 225. 

1 Sjrmpathetic nerve. 

8 Oesophagus. 

11 Jugular lymph sac. 

13 Jugular lymph sac, jugular approach. 

14 Jugular Ijrmph sac, subclavian approach. 
16 Dorso-medial somatic venous tributaries. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 

25 Internal jugular vein. 

26 Common jugular vein. 

29 Jugulo-subclavian trunk. 

30 Sixth spinal nerve. 

31 Primitive ulnar veno-lymphatic. 



FIGURES 64, 65 AND 66 

64 Same, section 31. 

65 Same, section 32. 

66 Same, section 33. 

1 Sympathetic nerve. 

12 Jugular lymph sac, thoracic duct approach. 

13 Jugular lymph sac, jugular approach. 

14 Jugular lymph sac, subclavian approach. 
22 Vagus. 

24 Thyrocervical artery. 

25 Internal jugular vein. 

29 Jugulo-subclavian trunk. 



FIGURES 67, 68 AND 69 

67 Same, section 35. 

68 Same, section 36. 

69 Same, section 38. 

1 Sympathetic nerve. 

12 Jugular lymph sac, thoracic duct approach. 

13 Jugular lymph sac, jugular approach. 

14 Jugular lymph sac, subclavian approach. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 

25 Internal jugular vein. 

29 Jugulo-subclavian trunk. 



FIGURKS 70, 71 AND 72 

70 Same, slide IX, section 2. 

71 Same, slide IX, section 5. 

72 Same, slide IX, section 6. 

1 Sympathetic nerve. 

12 Jugular lymph sac, thoracic duct approach. 

14 Jugular lymph sac, subclavian approach. 

22 Vagus. 

24 Thyrocervical artery. 

26 Common jugular vein. 



FIGURES 73, 74 AND 75 

73 Same, slide IX, section 9. 

74 Same, slide IX, section 10. 

75 Same, slide IX, section 11. 

1 Sympathetic ner\'e. 

8 Oesophagus. 

9 Trachea. 

12 Jugular lymph sac, thoracic duct approach. 

14 Jugular lymph sac, subclavian approach. 

16 Dorso«medial somatic venoua tributaries, 

22 Vagus. 

24 Thyrocervical artery. 

26 Common jugular vein. 



FIGURES 76, 77 AND 78 

76 Same, .slide IX, section 12. 

77 Same, slide IX, section 13. 

78 Same, slide IX, section 14. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

12 Jugular lymph sac, thoracic duct approach. 

16 Dorso-medial somatic venous tributaries. 

17 Prevertebral venous plexus. 
22 Vagus. 

24 Thyrocervical artery. 
26 Common jugular vein. 



EXPLANATION OF FIGURE 79 

79 Transverse section of left lower cervical region in a 15 mm. cat embryo 
(series 246, slide XI, section 24), X 225. 

1 Sympathetic nerve. 

8 Oesophagus. 

12 Jugular lymph sac, thoracic duct approach. 

14 Jugular lymph sac, subclavian approach. 

16 Dorso-medial somatic venous tributaries. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 
26 Common jugular vein. 



FIGURES 80, 81 AND 82 

80 Same, section 25. 

81 Same, section 26. 

82 Same, section 27. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

12 Jugular lymph sac, thoracic duct approach. 

14 Jugular lymph sac, subclavian approach. 

16 Dorso-medial somatic venous tributarieh. 

22 Vagus. 

23 Left carotid arterv. 

24 Thyrocervical artery. 
26 Common jugular vein. 



FIGURES So AND 80 

85 iSame, section 18. 

86 Same, section 20. 

1 Sympathetic nerve. 

12 Jup:ular lymph sac. thoracic duct approach. 

18 Jupular lymph sac, jujijular approach. 

14 Juguhar lymph sac. subclavian approach. 

21 Thymus. 

22 VagUis. 

24 Thvroccrvical artcrv. 
2o Internal jugular vein. 
29 Jugulo-subclavian trunk. 



FIGUIIES 87 AND HS 

87 Same, section 22. 
SS Same, section 24. 

1 Sympathetic nerve. 

12 Jugular lymph sac, thoracic duct approach. 

13 Jugular lymph sac, jugular approach. 

14 Jugular lymph sac, subclavian approach. 
16 Dorso-medial somatic venous tributaries. 

21 Th>Tnus. 

22 Vagus. 

24 Thyrocervical artery. 

25 Internal jugular h-mphatics. 
29 Jugulo-subclavian trunk. 



FIGURES 89, 90 AND 91 

89 Reconstruction of caudal end of left jugular lymph sac. with thoracic duct 
approach, in a 13.5 mm. cat embryo (series 189, slide VII. sections 1 to 50), X 225. 
Dorsal view. 

90 Reconstruccion of caudal end of left jugular lymph sac, with thoracic duct 
approach, in a 15 mm. cat embryo (series 245, slide XI, sections 1 to 44), X 225. 
Dorsal view. 

91 Reconstruction of caudal end of left jugular lymph sac with thoracic duct 
approach, in a 17 mm. cat embryo (series 142. slide X. sections 1 to 28. slide XI, ^ 
sections 1 to 29), X 225. Dorsal view. 

1 Sympathetic nerve. 
7 Aorta. 

12 Jugular lymph sac, thoracic duct approach. 

13 Jugular lymph sac, jugular approach. 

14 Jugular lymph sac, subclavian approach. 
16-46 Dorso-medial somatic venous tributaries. 

(Sup. intercostal v.) 

17 Prevertebral venous plexus. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 

25 Internal jugular vein. 

26 Common jugular vein. 
29 Jugulo-subclavian trunk. 

31 Primitive ulnar veno-lymphatic. 

33 Left subclavian artery. 

33' Left subclavian vein. 

35 Thoracic duct, preazygos segment. 

41 Vertebral arterv. 

42 Vertebral vein. 

46 Innominate artery. 

46 Left superior intercostal vein. 

54 Fifth spinal nerve. 

55 Sixth, seventh and eighth spinal nerve. 



1 Ua^KS 92 AND 93 

92 Dissection of the veins and lymphatics at the root of t lie neck in an aduM cat. 
(Xo. 67). 

93 Same, No. 13. 

(Figs. 92, 93, and 94 arc republished from Uuniingtou and McClure's ** Anatomy 
and Development of the Jugular Lymph Sacs in the Domestic Cat," Am. Jour. 
Anat., Vol. X, No. 2.) 



FIGUHK 94 
94 Same. No. .56. 



FIGURE 95 

05 Dissection of main lymphatic vcssols of neck and thorax in an a<luU cat 

(No. 22). 

1 External jugular vein and lymphatics. 

5 Subclavian vein. 

7 Internal mammary artery and lymphatics. 

S Broncho-mediastinal or ventral mediastinal lymphatic trunk. 

10 Cephalic vein and lymphatics. 

11 Vertebral vein. 

12 Thoracic duct, preazygos segment. 
15 Oesophagus. 

17 Internal jugular vein and lymphatics. 

18 Jugular approach and tap. 

19 Subclavian approach and tap. 

20 Innominate artery. 

21 Azygos vein. 



FIGURE 96 

96 Dissection of main lymphatic vessels of neck and thorax in an adult cat 

(No. 29). 

1 External jugular vein and lymphatics. 

2 Common jugular vein. 

3 Jugular lymph sac. 

4 Inferior thyroid lymphatics. 

5 Subclavian vein. 

6 Internal mammary lymphatics. 

7 Internal mammary artery. 

S Hroncho-mediastinal or ventral mediastinal lymphatic trunk 

9 Thyrocervical artery: 

10 Cephalic vein and l\^nphatic8. 

11 Vertebral vein. 

12 Thoracic duct, preazygos segment. 

13 Left subclavian artery. 

14 Junction of preazygos and azygos segments of thoracic duct, 
lo Oesophagus. 

16 Azygos segment of thoracic duct. 



FIGURE 97 

97 Dissection of main lymphatic vessels of neck and thorax in an adult cat 
(No. 131). 

1 External jugular vein and lymphatics. 

2 Common jugular vein. 
5 Subclavian vein. 

7 Internal mammary artery. 

8 Broncho-mediastinal or ventral mediastinal lymphatic trunk. 

9 Thyrocervical artery. 

12 Thoracic duct, preazygos segment. 

13 Left subclavian artery. 

15 Oesophagus. 

16 Azygos segment of thoracic duct. 

17 Internal jugular vein and lymphatics. 
20 Innominate artery. 

23 Innominate vein. 

26 Aorta. 

27 Vagus nerve. 

28 Inferior thyroid vein. 

29 Jugulo-cephalic venous trunk 



FIGURE »S 

98 Dissection of left jugular lymph sac and thoracic duct in an adult cat (\o. 
168). 

2 Common jugular vein. 

5 Subclavian vein. 

8 Broncho-mediastinal or ventral mediastinal lymphatic trunk. 

9 Thyro-cervical artery. 
13 Left subclavian arterv. 
15 Oesophagus. 

17 Internal jugular vein and lymphatics. 

18 Jugular approach and tap. 

21 Azygos vein. 

22 Trachea. 

23 Innominate vein* 

24 Vena cava superior 

25 lieft carotid artery. 



FKU'RK no 

M9 Schema showing composite picture of left juguhvr lymph sac, broncho iiu 
(liastinal trunk and preazygos segment of thoracic duct. 

1 External jugular vein and lymphatics. 

3 Jugular lymph sac. 

5 Subclavian vein. 

6 Internal mammary lymphatics. 

8 Broncho-mediastinal or ventral mediastinal lymphatic trunk. 

9 Thyro-cervical artery. 

10 Cephalic vein and lymphatics. 

11 Vertebral vein. 

12 Thoracic duct, preazygos segment. 

13 Left subclavian artery. 

10 Azygos segment of thoracic duct. 

17 Internal jugular vein and lymphatics. 

IS Jugular ai)i)roach and tap. 

19 Subclavian approach and tap. 

20 Innominate arterv. 

23 Innominate vein. 

24 Vena cava superior. 
2') Left carotid arterv. 
2() .\orta. 



DEVELOPMENT OF THE THORACIC DUCT 91 

The Development of the Broncho-Mediastinal Trunk and of the 

Preazygos Segment of the Thoracic Duct 

The area in which the development of the broncho-mediastinal 
and preazygos segments of the thoracic duct occurs is shown in 
fig. 100, which gives a topographical view of a transection of the 
upper thoracic region in a 12 mm. embryo (series 78, slide IX, 
section 5, X 50). 

The section includes the entire coelom ventrally, and the 
structures between it and the notochord dorsally. The right (S) 
and left {6) precaval veins occupy the lateral limits of the dorsal 
region. In the interval between them are seen the oesophagus 
(5), the trachea (9), the vagi {22) and the dorsal aortic arches 
(7). Dorsal to the main veins on each side are the strands of the 
brachial plexus (not labelled in the figure), and dorsal to the 
nerves is the primitive ulnar veno-lymphatic (Si). Further 
mesad follow the subclavian arteries {33), the entrance of the 
dorso-medial venous tributaries {16) into the main veins, and the 
sympathetic strands (i). The letter Y in the figure, between 
the notochord and the dorsal mediastinal structures named, 
indicates the center of the area in which the development of the 
preazygos segment of the thoracic duct will proceed in the succeeding stages. 

The ventral portion of the field contains the coelom, with right 
{IfS) and left {J^O) auricles, right ventricle {50), ascending aorta (7) 
and ascending trunk of main pulmonarj'^ arter>' {10), Dorsal to 
this are seen the cross-sections of the right and left pulmonary 
arteries {10) descending to the lun^s. Between them ventrally, 
and trachea (9), aortae (7), vagi {22) and praecaval veins (S, 6) 
dorsally, is the area marked by the letter X, in which the development of the broncho-mediastinal trunk will proceed. 

A. The developynent of the broncho-ynediastinal or ventral mediastinal lymphatic channeh, which drain subsequently caudo-sinistrad 
into (lie left thoracic duct, or cephalo-sinistrad into the subclavian 
approach of the jugular lymph sac, or into both. 

In the earlier stages (embrj^os of 11-14 mm.), an extensive 
ventral venous capillary network develops between the main 



92 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

venous trunks of the right and left sides, involving the distal part 
of the internal jugular, the common jugular and the innominate veins. 

Out of this general antecedent sinistro-dextral ci^illary reticulum the definite retro- or suprathymic innominate anastomosis 
develops subsequently in normal individuals, but in the earlier 
stages this plexus extends both ventral and dorsal to the thymus 
anlage. 

The venous network develops, in addition to the prevertebral 
and dorsal somatic components, chiefly on the lateral aspect of the 
oesophagus, in the peri-tracheal area, and around the thymus and 
the common carotid artery. It trends cephalo-laterad towards 
the main venous line (jugulo-innominate), into whose mesal surface the terminals of the plexus discharge. 

In so doing they encounter, and partially surround, the sympathetic and vagus nerves, and the thymus body. Consequently 
the terminal branches of this ventral mediastinal plexus enter 
the main vein both ventral and dorsal to these three structures 
and through the intervals between them. Thus the composite 
plan of this venous area appears as shown in the schematic fig. 
101, which represents the combination of a number of transverse 
sections of the anterior thoracic region. 

The terminal connections of the ventral mediastmal plexus 
may be grouped in reference to their derivation and their relation 
to adjacent fields of venous drainage into the following five sets, 
(fig.fOl): 

1. Dorso-medial somatic tributaries of internal and common 
jugular and of innominate veins (fig. 101, 16) entering the main 
venous channel dorsal to the sympathetic nerve, and frequently 
combined with 

2. Terminal of prevertebral venous plexus anterior to azygos 
veins (fig. 101, 17). 

3. Terminal of peritracheal plexus passing laterad between 
sympathetic {1) and vagus {22) nerves (fig. 101, 18). 

4. Ventral mediastinal branch, draining, as "suprathymic 
plexus," the area between the thymus {21), carotid {23) and 
vagus {22) . This is the line of the future typical permanent left 
innominate anastomosis dorsal to the thymus (fig. 101, 19). 



DEVELOPMENT OP THE THORACIC DUCT 93 

5. Subthymic plexus, passing ventral to the thymus anlage 
(fig. 101, SO). This forms, if retained and further developed in 
the adult, the occasionally observed '*prethymic" left innominate 
vein ^'*\ 

Any number of good examples of all these conditions are afforded 
by every 13 or 14 mm. embryo. Thus in a 14 nun. embryo 
(series 210, slide viii, section 41, X 225), fig. 102, direct comparison of the schema shown in fig. 101 with the section will, 
without further description, make the arrangement of the elements composing this plexus (16, 17, 18, 19, 20) clear. (Compare also fig. 43 [series 189, slide vh, section 10, 13.5 mm.] 
and fig. 30 [series 210, slide viii, section 39, 14 mm.]) 

The ventral divisions of this plexus extend in the earlier embryonic stages (11-12 nun.) as a well developed capillary reticulum into the upper thoracic region around and between oesophargus, trachea, precardinal veins, vagi and pulmonary arteries. 

Beginning in some 12 nun. embryos, but more constantly and 
characteristically in the 13 nun. stage, certain components of this 
ventral mediastinal venous plexus appear partly surrounded by 
independently developed extraintimal lymphatic spaces, which 
form the anlages of the future broncho-mediastinal lymphatic 
trunk. 

Thus, if the ventral portion of this venous plexus is followed 
caudad into the upper thoracic region, into the area of the developing broncho-mediastinal trunk marked X in fig. 100, the following 
observations can be made in stages of the proper length, and 
adequately fixed and stained: 

1. In embryos between 11 and 12 nmi. only venous capillaries 
are found. Thus figures 103 and 104 show transverse sections 
of this part of the upper thoracic region in a 12 nmi. embryo 
(series 217, slide viii, sections 21 and 29, X 200). The field, 
caudal to oesophagus and aorta (7), contains in the middle hne 
the trachea (S), the vagi {22), and further ventrad, the pulmonary 



•• Geo. S. Huntington : Contribution to the topographical anatomy of the thorax 
in the foetus at term and the new-bom child." Rep. Soc. N. Y. Lying-inHospital, 1897, p. 343, fig. xxxi. 



94 DEVELPPMENT OF THE STSTEBilC LYMPHATIC VESSELS 

arteries (10). The branches of the peritracheal venous plexus 
(18) are well developed. There is as yet no indication of lymphatic development. 

2. In 13 mm. embryos certain of the venous radicles entering 
into this plexus, are partly surrounded and enveloped by extraintimal lymphatic spaces, which arise independently of the 
venous system, as the first anlages of the future ventral mediastinal lymphatic channel. Figures 105 and 106 show transverse 
sections of this region in a 13 mm. cat embryo (series 92, slide 
vii, sections 30 and 38) in a magnification of 225 diameters. 
Ventral to trachea (9), aorta (7) and left vagus {2£) are seen sections of a number of venous radicles (4) of the ventral mediastinal 
plexus, some of which are partially surrounded by very smiall 
extraintimal perivenous lymphatic anlages (5). Only a few of the 
most prominent of these are indicated in the figures by leaders, 
but they exist in many other parts of the field. 

A similar section from another 13 nmi. embryo (series 107, 
slide ix, section 40, X 225) is shown in figure 107. Dorsal to 
the pulmonary arteries (10), between them and the trachea (9) 
and aorta (7), the section has cut a prominent extraintimal lymphatic space (5) in typical relation to one of the radicles (4) of 
the ventral mediastinal venous network. 

3. In the 13.5 mm. embryo the full and convincing proof of 
the extraintimal derivation of this channel is given. In some 
embryos of the period the process is still seen in its earlier stages. 
Thus figs. 108 and 109 (13.5 mm. embryo, series 223, slide x, 
sections 11 and 12, X 225) show on each side, ventral to the 
trachea (9) and the vagi (22) y a number of radicles (4) of the ventral mediastinal capillar}^ plexus. One of these small vessels, 
symmetrically disposed on each side in front of the respective 
vagus, is in process of being surrounded and replaced by an extraintimal lymphatic space (5). 

Other 13.5 mm. embryos show a rapid advance in the perivenous Ijinphatic development. 

Fig. 110 shows a transverse section of the upper thoracic 
region of another 13.5 mm. embryo (series 189, slide viii, section 
35, X 225). Just ventro-mesad of the left vagus nerve and its 



DEVELOPMENT OF THE THORACIC DI3CT 95 

encircling vein is a venous radicle (4) almost completely surrounded by an extraintimal lymphatic space (5) in the process 
of replacing the atrophying vein with which it is so closely associated. The same structures (4, 5) are seen still more clearly 
defined in the corresponding position on the right side of the 
embryo. 

Comparison with tl\e corresponding sections just given in figures 
103 to 109 show that the extraintimal anlage of the earlier stages, 
developed along the identical venous radicle, has increased in the 
13.5 nrni. stage, so as to nearly envelop the vein, and that the 
latter, if followed cephalad and caudad, is now separated from 
the functional venous channels of this region and is in the process 
of further recession and degeneration as the lymphatic perivenous 
space enlarges and more and more replaces the antecedent venous 
channel. The vein in question in the older embryo (series 189) 
appears collapsed and shrunken, and contains only a few degenerating red blood cells. In the same situation on the right side 
of fig. 110 (series 189, slide viii, section 35), the section has cut 
the corresponding vein and the enveloping extraintinr al space at 
right angles, so that the central kernel of the shrinking vein (4), 
still containing a few degenerating red blood cells, is nearly completely surrounded by the replacing extraintimal lymphatic (5). 

Fig. Ill shows the following section of the same embryo (series 
189, slide viii, section 36), magnified 225 diameters, in a larger 
field which gives the topographical relations and may serve in 
in the orientation of the succeeding plates. The ventral circumference of the oesophagus iS) and the aorta (7) are seen dorsally. 
The trachea (9), with the vagi {22) on either side, occupies the 
central area. Ventrally are the two pulmonary arteries {10). 
The section is a most important one in interpreting the early 
histogenetic stages of the broncho-mediastinal lymphatic trunk 
and its relation to the embryonic mediastinal venous plexus. 
The same venous radicle (4), ventral to the vagus {22), already 
noted in the preceeding section (fig. 110), is seen on each side. 
On the left side it has been cut obliquely by the plane of the 
section, and hence shows a segment of considerable length, as 
a practically empty and partially collapsed endothelial bag (4), 



96 DEVEIiOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

surrounded by the extraintimal lymphatic space (6). On the 
right side of the embryo the corresponding venous radicle (4) 
and the perivenous lymphatic anlage (6) have been again cut 
more at right angles, so that the envelopment of the former by 
the latter can be clearly traced nearly throughout the entire circimiference. 

Fig. 1 11 A shows the decadent vein and the replacing extraintimal lymphatic on the left side of this section in a higher magnification, ( X 300). The structure of the collapsed venous endothelial 
tube, and the beginning development of endothelial character in 
the mesodermal cells limiting the perivenous extraintimal lymphatic anlage, can be here clearly made out. 

Figs. 112 to 116 show the five succeeding sections of the same 
embryo (series 189, slide viii, sections 37 to 41 inclusive) in a 
magnification of 225 diameters. 

I publish this series of plates in order to prove on the one hand 
that the extraintimal lymphatic anlages can be followed with 
certainty and accuracy in their relation to the contained decadent 
venule for longer or shorter distances, and that, on the other 
hand, they are, in these earlier stages, still isolated and not yet 
continuous with similar anlages in adjacent areas. They form, 
in other words, in these earlier periods, detached links of a lymphatic chain, not yet united to each other to form the continuous 
channel of the later stages. 

In figs. 112, 113 and 114 (sections 37, 38 and 39) beautiful and 
clear pictures of the atrophying central venule (4) and the perivenous extra-intimal lymphatic space (5) are found on both sides 
in the typical situation noted in the preceding sections, with 
which they of course can easily be coordinated by simple comparison. 

Sections 38 and 39 (figs. 113 and 114) are particularly instructive inasmuch as the detached central vein (4) on the left side 
still contains a few degenerating red blood cells, while its former 
connection with the vahd and functional venous plexus around 
the left vagus nerve can still be faintly traced. 

In section 40 (fig. 115) the atrophying vein (4) and the surrounding lymphatic (5) of the left side appear divided into two 



DEVELOPMENT OP THE THORACIC DUCT 97 

components. On the right side the corresponding structures end 
blindly. 

In the following section (41, fig. 116) the left venule and lymphatic also terminate almost entirely in the indifferent mesodermal tissue, only a small renmant (4, 5) persisting between trachea 
and left vagus. This disappears entirely in the following section. 

The succeeding stage (14 mm.) shows the same lymphatic 
anlages surrounding and replacing the atrophying venules of the 
ventral mediastinal plexus in still higher development. It appears from the study of numerous embryos of this length, that 
the average 14 mm. stage represents the point in the lymphatic 
ontogenesis of this region at which the pictures are most striking. The central kernel of the decadent vein is still large and, 
in places, as yet incompletely separated from the definite venous 
channels. At the same time the perivenous lymphatic space has 
acquired an increased lumen and hence the two combined structures occupy a relatively large field. 

Thus figs. 117 to 122 show transverse sections of the ventral 
thoracic region in a 14 mm. cat embryo (series 212, slide x, sections 4, 5, 6, 7, 10 and 11, X 225). In figs. 117 and 118 the 
developing lymphatic anlages (5) of the broncho-mediastinal 
trunk can ke readily recognized and present the same relation 
to the atrophying venules, which they surround-, as in the sections 
of the preceding series just described and figured. In contradistinction to these structures the components of the permanent 
functional venous plexus of this region {32) form well-differentiated vascular channels. 

In fig. 119 (series 212, slide x, section 6) the scattered lymphatic anlages occupying in the two preceding sections the space 
between the left pulmonary artery {10) and the left vagus {22) j 
with its accompanying ventral mediastinal vein {32) j are gathered 
together into a more extensive elongated space (5). In the 
interior of this is seen the endothelial bag of the empty and 
atrophying venule (4) which the lymphatic is about to replace. 
The vein renmant is almost completely surrounded by the lymphatic space and only connected to the latter's endothelial wall 
by a bridge at one point. Other areas of similar lymphatic devel


98 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

opment are seen on the opposite side {4-5) and (not labelled) in 
the center of the field, but the structures on the left side are, 
as in the earlier stafres (cf. series 189) better developed and 
larger. 

The succeeding figures, 120, 121 and 122 (sections 7, 10 and 
11) show the same structures, which can be distinctly followed 
for some distance caudad of the last section figured. In fig. 122 the 
original connection of the large upper venous kernel of the left side 
(4) with one of the components of the peritracheal venous plexus 
(18) is still suggested By the arrangement of the adjacent cells, 
although the degenerating vein has been cut off from all actual 
communication with the permanently valid channels of the 
mediastinal venous plexus. 

The 14 mm. stage is so important, and the results gained by 
the examination of a laige number of embryos so conclusive in 
respect to the true ontogenesis of the systemic lymphatic channels, 
that I have selected a well marked example and pubUsh here 
eighteen consecutive, or nearly consecutive, sections from the 
same individual. I do this in order to show the extent to which 
extraintimal perivenous lymphatic development has proceeded 
in this stage, in respect to the length of the resulting segments of 
the future lymphatic channel, still separated from each other, 
and to accentuate, by a large number of successive illustrations 
from the same embryo, the histogenesis of the lymphatic anlages 
in their relation to the decadent embryonic venules which they 
eventually entirely replace. The conception involved by the 
theory of extraintimal systemic lymphatic development has 
proved apparently, to judge from published comments, difiScult 
to understand in some laboratories from the histo-mechanical 
standpoint. The following eighteen reproductions of sections 
of a 14 mm. embryo (series 214, slide xiii) surely explain, without detailed description, the principles underlying lymphatic 
ontogenesis in the mammalian embryo. I very gladly welcome 
the opportunity, which this series of Wistar publications offers, 
for presenting them. 

The plates comprised in this group are shown in order cephalocaudad in figures 123 to 141 inclusive. In all of them the ex


DEVELOPMENT OP THE THOHACIC DUCT 99 

traintimal lymphatic anlages of the broncho-mediastinal trunk 
are indicated by the leader 5, while the included remnant of the 
atrophying embryonic vein is labelled 4, as in the preceding 
and following figures. 

Figs. 123, 124, 125 and 126 (sections 4, 5, 6 and 7) show well the 
relation of the venule (4), undergoing atrophy and replacement 
by the extraintimal lymphatic space (5), to the permanent 
venous channels of the mediastinal plexus. Thus in fig. 123 the 
dorsal large lighter area marked 4 is the blind cephalic end of a 
venule which is nearly detached from the permanent peritracheal 
(18) and ventral mediastinal (32) venous channels, and which in 
the succeeding sections is seen to be partially surrounded by the 
extraintimal lymphatic space (5) eventually designed to replace 
it entirely. 

In figure 124 (section 5) this perivenous space (5) has developed. 
The included vein (4) is still partially connected with the functional peritracheal plexus (18). Further ventrad is another portion of this same plexus. The venous kernel here still contains a 
number of red blood-cells. These characteristic relations of 
developing lymphatic and receding vein can be followed clearly 
throughout the succeeding sections. The contrast between the 
well filled permanent veins {e.g.j 18, 32 in figs. 123, 124, 125 
and 126), with walls fitted closely into the surroimding mesenchyme, and the atrophying venule surrounded by the extraintimal 
lymphatic anlage, is striking throughout the series. Some of the 
sections show in certain regions good pictures of nearly complete 
reduction of the decadent vein to an insignificant central kernel 
of connective tissue surrounded by the extraintimal lymphatic 
space; thus, e.g., figs. 137 to 141 in the region ventro-mesad to 
the left vagus {22). 

The 15 nma. stage shows the developing lymphatic plexus of 
the broncho-mediastinal trunk further advanced. Figs. 142 to 
145 show four successive transverse sections through the ventral 
part of the upper thoracic region in a 15 mm. cat embryo (series 
216, slide x, sections 32, 33, 34 and 35, X 225). The central 
decadent venule in the interior of the developing perivenous 
lymphatic space has in many places disappeared entirely, leav


100 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

ing only the clear lymphatic lumen (5). In other places remnants 
of the replaced vein (4) can still be distinctly determined. This 
clearance has resulted in a relative diminution of the actual area 
of a cross section of the meshes of the lymphatic plexus, since now 
the entire lumen is given over to the newly formed lymphatic 
channel, whereas in the earlier stages its central area was still 
largely filled by the degenerating veil. The lymphatic spaces 
in these sections have increased considerably in number. (Only 
a few of the more prominent vessels are indicated m the figures 
by leaders.) 

A transverse section of this region in a 16.^ mm. cat embryo 
(series 215, slide xiv, section 31, X 226) is shown in a fig.146. 
The preceding more diffuse lymphatic plexus of the earlier stages 
is condensed to a much smaller mesenchymal network. In a 
few of the larger meshes a remnant of the former central vein (4) 
can still be traced as a solid plug of mesoderm surrounded by the 
lymphatic channel (5). 

In general the 15 and 15.5 mm. embryos of the cat represent 
the stages in the development of the broncho-mediastinal trunk 
in which the histological pictures of the lymph channels are least 
distinct aod striking. This is due to the fact that on the one 
hand they have lost the central venous kernel around which they 
were originally developed through confluence of extramthnal 
spaces, and which gave to the combined structures their area 
on section and their distinctive appearance in the earlier (13.5 
and 14 mm.) stages, while on the other hand the independent 
growth and enlargement of the lymph channels proper begins in 
the 16 mm. stage. In some embryos, measuring 16 mm., the 
appearances characteristic of the 15 mm. and 15.5 mm. stages are 
still encountered. Thus fig. 147 shows a transverse section 
through the ventral area of the upper thoracic region in a 16 mm. 
embryo (series 230, slide xii, section 25, X 225). The correspondence of the histological picture to that presented by the 
15 mm. or 15.5 mm. embryo is seen by comparison with series 
215 and 216 (figs. 142 to 146). 

The majority of 16 mm. embryos show, however, a marked 
advance in the independent growth of the lymphatic channels, 



DEVELOPMENT OF THE THORACIC DUCT 101 

which have become fully established. Their lumen now appears 
for the most part entirely cleared of the remnants of the decadent 
venules originally contained therein. In only a few instances 
does the original vein kernel appear reduced to an insignificant 
rudiment. The resulting plexus of the broncho-mediastinal lymphatic duct fills the typical position occupied in the earlier stages 
by the extensive preceding perivenous lymphatic reticulum. 
Thus figs. 148-153 give transverse sections through the ventral 
part of the upper thoracic region in another 16 mm. cat embryo 
(series 222, sUde X, sections 1, 2, 3, 10, 15 and 16, X 225). This 
embryo affords remarkably clear pictures of the fully developed lymphatic plexus of the ventral or broncho-mediastinal 
trunk. 

Figs. 148 and 153 (sections 1 and 16) give the topographical 
pictures of the entire region involved. The broncho-media^^tinal 
lymphatic plexus {37) is fully developed in the typical area between 
the trachea (5) and vagi (32) dorsally and the pulmonary arteries 
(10) ventrally. The lymphatic spaces possess a clear lumen and 
distinct endothelial walls. The remnants of the degenerating 
ventral mediastinal venous plexus which they have replaced have 
almost entirely disappeared. Only slight traces of them are 
still to be seen here and there. In the main the lymphatic channels are clear of venous kernels and form a rich interlacing lymphatic plexus. The central field contains the oesophagus (5), 
aorta (7) and part of the medial circumference of the left praecava 
(6). Dorsally on the right side the right azygos vein (S) and 
sympathetic nerve (1) appear, while on the left side the section 
includes the cephalic part of the azygos segment of the left thoracic 
duct (36). 

Sections 2, 3, 10 and 15 of the same slide are shown in their 
ventral portions in figs. 149 to 152. They all exhibit the extent 
and continuity of the broncho-mediastinal lymphatic channel 
complex in this stage. The figures are not leadered, but the 
individual structures can be readily identified by reference to 
the topographical figures 148 and 153. 

The succeeding stages are characterized by a condensation of 
the extensive lymphatic plexus of the typical 16 nmi. and 17 mm. 



102 DEVELOPMENT OP THE SYSTEMIC LYMPHATIC VESSELS 

embryos into the more definite channel of the broncho-mediastinal 
trunk with larger caliber. 

Figs. 154 to 158 show the region of the broncho-mediastinal 
channel in four successive sections in a 20 mm. cat embryo 
(series 241, slide xix, sections 19, 20, 21 and 22, X 225). Fig. 
154 again gives a topographical view of the entire field, while 
the same is cut down to the ventral portion in the remaining plates. 
In all the multi-meshed lymphatic plexus of the preceding stage 
is replaced by the more definite and larger channel of the bronchomediastinal trunk proper (37) y in the classical situation between 
the pulmonary arteries (10) ventrally and the trachea (9), vagi 
(SS) and permanent ventral mediastinal veins (18) dorsally. 

This stage marks the practical attainment of adult conditions 
for the lymphatic channel of the broncho-mediastinal trunk, and 
from this period on its further development is merely a question 
of continued growth and adaptation to the environment in establishing secondary connections with the tributary channels, 
developed independently, the preazygos segment of the thoracic 
duct, and (usually) the ventral prolongation of the subclavian 
approach of the jugular lymph sac. 

As will be seen from the foregoing analysis of the development 
of the broncho-mediastinal lymphatic trunk in embryos of the 
cat, the principles of mammalian systemic lymphatic ontogenesis 
defined in Part I of this memoir are consistently sustained by 
the actual evidence afforded. The development of the perivenous extraintimal anlages which form the basis for the subsequent evolution of the systemic lymphatic channels, is a uniform 
and remarkably consistent process. 

The existence of these spaces in this and other regions of the 
embryo has been so often denied by recent contributors to the 
subject, or, if admitted, explained in every possible way except 
through the correct- interpretation, that I pubUsh in this paper 
a series of micro-photographs of a considerable number of sections taken from embryos of all the important stages. Of course 
these observations could be indefinitely multiplied. The larger 
the embryological collection, and the better the individual preparations are fixed and stained, the more conclusive will be the 



DEVELOPMENT OP THE THOHACIC DUCT 103 

results of a careful examination of lymphatic development along 
the lines here indicated. 

No competent and impartial observer can mistake the significance of the conditions here shown. Every stage of the process 
can be followed in detail. The behavior of the decadent embrvonic vein, and its relation to the enveloping extraintimal lymphatic 
channel, are absolutely demonstrated. The endothelium of the 
shrinking, vein has no share in furnishing the independent lymphatic endothelimn of the replacing mesenchymal space, and 
nowhere, in the entire process, is there the faintest suggestion 
of an "out-bud" or of a "splitting ofif" from the circumference of 
an otherwise vaUd embryonic vein of "lymphatic'' or "venolymphatic'' anlages. 

It is evident in comparing a number of embryos between 13 
and 16 mm., crown-rump measure, that the extensive area occupied by the lymphatic anlages in the earlier stages (13 mm., 13.5 
mm. and 14 mm.) is due to the relatively large size of the central 
decadent vein. In the earlier stages {e.g., figs. Ill, 112, 113, 114, 
119, 121, 125, 126, 127, series 189, 212 and 214) the evacuated and abandoned vein appears as a wide loose and partially 
collapsed endothelial bag, surrounded by a narrow extraintimal 
lymphatic space, with but as yet indifferently defined endothelial 
lining, continuous at one or more points with the external surface 
of the endothelium of the degenerating vein. As development 
proceeds the actual perivenous lymphatic spaces increase but they 
concentrate and narrow down on the contained venous kernel, 
and, as the latter continues to decrease in size and finallj^ become 
completely eliminated, the resulting clear lymphatic channel occupies relatively less space than that filled in the earlier stages 
by the decadent venule and the early surrounding lymphatic 
anlage combined. 

Thus in the 15, 15.5 and in some 16 nmi. embryos (figs. 142, 
143, 144, 145, 146, and 147, series 216, 215 and 230), while the 
actual lumen of the lymphatic channel has increased that of the 
enclosed and abandoned vein has corresponding!}^ receded to an 
insignificant remnant, which projects into the lymphatic space 
from a narrow pedicle attached to the latter's endothelial lining. 



104 DEVELOPMENT OP THE SYSTEMIC LYMPHATIC VESSELS 

Consequently, in the pictures of the earlier stages (13, 13.5 and 
14 mm. embryos) the area occupied by the still capacious abandoned venous channel, combined with that of the relatively narrow 
enveloping lymphatic space, appears larger and more prominent 
than in the later periods (15, 15.5 mm.) in which the permanent 
lymphatic channel and its reduced venous kernel occupies less 
histological territory. 

It should also be noted that in the earlier stages (13, 13.5, 
14 mm.) the perivenous extraintimal lymphatic network is more 
diffuse and redundant than in the later stages (15, 15.5, 16 mm.). 
This early plexiform lymphatic reticulum is subsequently condensed into more limited and better defined lymph channels, in 
exact conformation to the processes observed in the haemal 
vascular development, in which the definite blood channels 
crystallize along main lines out of an antecedent indefinite and 
more diffuse plexus. The result of this genetic process is strik; 
I ing in tracing developing lymphatics through successive stages. 

Thus in the region here imder discussion the pictures offered by 
the 13, 13.5 and 14 mm. embryos are more conclusive than those 
furnished bj' the 15 and 15.5 mm. stages in reference to the genesis of the Ijonphatic channels. In the former, the lymphatic 
anlages and the decadent venules around which they develop are 
taken together, relatively larger and more numerous, and hence 
easier to recognize. In the latter, this early redimdant perivenous lymphatic plexus has been replaced by a relatively smaller, 
but much more definite and distinct channel, occupjdng, however, 
always a part of the area filled in the earlier stages by the less 
circumscribed antecedent lymphatic plexus with its contained 
remnants of abandoned embryonic veins. I lay special stress on 
this fact, because it is absolutely neoessarj' to take it into account 
in comparing stages between 13.5 and 15.5 nmi. In the latter 
stage the final IjTiiphatic anlages have definitely formed and have 
reached the relation to adjacent main venous lines which they 
henceforth are to occupy. The further growth and enlargement 
of these chamiels begins in the 16 mm. embrj'o, and proceeds 
from this point on, in many regions at the expense of the adjacent 
embryonic vein undergoing atrophy. 



DEVELOPMENT OF THE THORACIC DUCT 105 

The only conclusion which seems to me to be warranted by 
actual observation is that certain embryonic veins form, during 
the process of their atrophy and final elimination from the definite 
venous organization, the supporting lines along which certain 
of the perivenous extraintimal lymphatic anlages first develop. 

The fact that numerous early embryonic venous channels, 
large and small, atrophy and disappear during the normal course 
of subsequent development, appears to afiford a more favorable 
field for the greater development of the adjacent mesenchymal inintercellular spaces, so that these enlarge more rapidly, as the correlated vein recedes. This relationship appears, however, to be 
based exclusively on the physical and mechanical advantages which 
the abandoned and shrinking primary venous line affords to the 
adjacent mesenchymal spaces for more rapid enlargement, in 
the sense of replacing the disappearing vein and occupying secondarily the space formerly filled by the haemal channel. This is 
evidently an important factor in determining the size and extent 
of the final lymphatic channel resulting from the confluence of 
the originally separate and independent perivenous anlages. 
Consequently, in the adult, the largest and best defined systemic 
lymphatic vessels either accompany reduced adult remnants of a 
relatively larger embryonic venous channel, or, in case of the 
latter's entire default, topographically replace the same. Now, 
while this relation manifests itself strikingly in many parts of 
the body, it is quite evident that the development of lymphatic 
chaimels occurs in other parts independently of preceding veins, 
by the confluence of independent intercellular mesenchymal 
spaces. 

The cat may, and does, differ in its details of lymphatic development, and in its adult lymphatic organization, from the conditions obtaining in many other mammalian forms. In fact, even 
in the present very incomplete state of our knowledge of the comparative anatomy of the mammalian lymphatic system, we 
realize that what we regard as the mammaUan ground plan of 
lymphatic organization may in certain genera undergo great and 
far-reaching modifications, as for example the conditions deter


106 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

mined by Silvester'^ for the whole group of the Cebidae, and those 
found by myself in Macropua rufus. And yet these diflferences, 
established and maintained within the natural limits of the 
mammalian class, cannot, in whatever degree they actually exist, 
in individual forms be basic. In any given mammalian type, 
the systemic lymphatic vessels, whatever their adult relation to 
and connection with the venous system may be, must develop 
in accordance with a genetic groimd plan common to all mammalia. 



•' C. F. Silvester. On the Presence of Permanent Lymphatico-Venous 
Communications at the Level of the Renal Veins in Adult South American 
Monkeys." 

AnaU Am,, Erganzungsh. z. 37. Bd., Vevh. Anat. Ges., 24 Vevs., Brttssels, 
1910, S. 111-114. 



PART II PLATES 

FIGURES 100 TO 158 



FIGURE 100 

100 Transverse section of upper thoriicic region in a 12 mm. cat embryo (series 
78f slide IX, section 5), X 50. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

6 Precardinal or precava, resp. azygos of left side. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 

10 Pulmonary artery. 

16 Dorso-medial somatic venous tributaries. 

22 Vagus. 

31 Primitive ulnar veno-lymphatic. 

33 Subclavian artery. 

48 Right auricle. 

49 Left auricle. 

50 Right ventricle 



FIGURE 101 

101 Schema of venous plexuses of left side in lower cerviciil region of cat embryo 
between 13 mm. and 14 mm. crown-rump measure in transverse section. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

16 Dorso medial somatic venous tributaries. 

17 Prevertebral venous plexus. 

18 Feri tracheal venous plexus. 

19 Suprathymic venous plexus. 

20 Subthymic venous plexus. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 
20 Coiiunon jugular vein. 



FIGURE 102 

102 Transverse section of lower cervical region in a 14 mm. cat embryo (series 
210, slide VIII, section 41) , X 225. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

16 Dorso-medial somatic venous tributaries. 

17 Prevertebral venous plexus. 

18 Peritracheal venous plexus. 

19 Suprathymic venous plexus. 

20 Subthymic venous plexus. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 

24 Thyrocervical artery. 

25 Internal jugular vein. 



FIGURES 103 AND 104 

103 Transverse section of ventral part of upper thoracic region in a 12 mm. cat 
embryo (series 217, slide VIII. section 21), X 200. 

104 Same, section 29. 

7 Aorta. 

9 Trachea. 

10 Pulmonary artery. 

IS Peritracheal venous plexus. 

22 Vagus. 



FIGUKES 10.-) AND 106 

105 Transverse section of ventral part of upper thoracic region in a 13 mm. cat 
embryo (series 92, slide VII, section 30), X 225. 

106 Same, section 33. 

3 Right precaval vein. 

4 Atrophying embryonal vein, fonning kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerating 

embryonal vein. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 
22 Vagus. 



FIGURE 107 

107 Transverse section of ventral part of upper thoracic region in a 13 mm. cat 
embryo (series 107, slide IX, section 40), X 225. 

3 Right precaval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing Ijinphatic space. 

5 Extraintimal or perivenous hmiphatic space surrounding degenerating 

embryonal vein. 
7 Aorta. 
9 Trachea. 
10 Puhnonarv arterv 



FIGURES 108 AXD 109 

108 Transverse section of ventral part of upper thoracic region in a 13.5 mm. 
cat embryo (^series 223, slide X, section 11), X 225. 

109 Same, section 12. 

• 4 Atrophying embryonal vein, fonning kernel in interior of developing 

and replacing lymphatic space. 
5 Kxtraintimal or perivenous lymphatic space surrounding degenerating 

embryonal vein. 
7 Aorta. 
9 Trachea. 
22 Vagus. 



FIGURES 110 AND lllA 

110 Transverse section through ventral part of upper thoracic region in a 13.5 
mm. cat embryo (series 189, slide VIII, section 35), X 225. 

111 A Left part of section 36 of same embryo, shown in the following figure 
111, X300. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerating 

embrvonal vein. 



FIGURE 111 

111 Transverse section through ventral part of upper thoracic region in a 
13.5 mm. cat embryo (series 189, slide VIII, section 36), X 225. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerating 

embryonal vein. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 

10 Pulmonarv artorv. 
22 Vagus. 



FIGURES 112 AND 113 

112 Same, section 37, X 225. 

113 Same, section 38, X 225. 

4 Atrophying embryonal vein, fonning kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degener
ating embryonal vein. 



FIGURKS 114 AND 115 

114 Same, section 39. X 225. 

115 Sjime, section 40, X 225. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraiutimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 
10 Pulmonarv arterv. 



FIOUHKS IH) AND 117 

116 Same, section 41, X 225. 

117 Transverse section through ventral part of upper thoracic region in a 14 
mm. cat embryo (series 212, slide X, section 4h X 225. 

3 Kight precaval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Kxtraintimal or perivenous h'mphatic space surrounding degenerat
ing embryonal vein. 

7 Aorta. 

9 Trachea. 
10 Pulmonar)' artery. 
22 Vagus. 
32 Ventral nr'diastinal venous plexus. 



FIGURES 118 AND 119 

118 Same, section 5. 

119 Same, section 6. 

3 Right precaval vein. 

4 Atrophying embryonal vein, fonning kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 

7 Aorta. 

9 Trachea. 
10 Pulmonary artery. 
22 Vagus. 
32 Ventral mediastinal venous plexus. 



FIGURES 120 AND 121 

120 Same, section 7. 

121 Same, section 10. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 

7 Aorta 

9 Trachea. 
10 Pulmonary artery. 
22 Vagus. 
32 Ventral mediastinal venous plexus. 



FIGURES 122 AND 123 

122 Saiiio. section 11. 

123 Transverse section through ventral part of upper thoracic region in a 14 mm. 
cat embryo (series 214, slide XIII, section 4) X 225. 

4 Atropliying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Kxtraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 

7 Aorta. 

9 Trachea. 

10 Pulmonary artery. 

18 Peritracheal venous ])lexus. 

22 Vagus. 

32 Ventral mediastinal venous plexus. 



FIGURKS 124 AND 120 

124 Same, section o. 

125 Same, section 0. 

3 Right precaval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 

7 Aorta. 

9 Trachea. 

10 Pulmonary artery. 

18 Peritracheal venous plexus. 

22 Vagus. 

32 Ventral mediastinal venous plexus. 



FKU'RKS llV) AND 127 

120 J:*:Linc, section 7. 
127 Same, section S. 

3 Kipht j)reciiviil vein. 

4 Atrophying enibryoniil vein, forming kernel in interior of <leveloping 

and replacing lymphatic space, 
o Kxtraintimal or perivenous lymphatic space surroinuling degenerating embrj'onal vein. 
7 Aorla. 
Trachea. 
10 Pulmonary artery. 
22 Vagus. 
32 Ventral mediastinal venous plexus. 



FKiUHES Vis AM) \2^ 

12S Same, sor-tioii 10. 
129 Sanio. section 11. 

3 Kiglit prcK'aval vein. 

4 Atrophying embryonal vein, fonuing kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous hinphatic space surrounding degenerat
ing embryonal vein. 

7 Aorta. 

9 Trachea. 
10 Pulmonary arterv. 
22 Vagus. 



FIGURES 130 AND 131 

130 Same, section 14. 

131 Same, section 15. 

3 Right preraval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous l>^nphatie space surrounding degenerat
ing embryonal vein. 

6 Precardinal or precava, resp. azygos of left side. 

7 Aorta. 

9 Trachea. 
10 Pulmonary artery. 
22 Vagus. 



FIGURES 132 AND 133 

132 Same, section 16. 

133 Same, section 17. 

3 Right precaval vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing Ijrmphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 
9 Trachea. 
10 Pulmonary artery. 
22 Vagus. 



FIGURES 134 AND 135 

134 Same, section IS. 

135 Same, section 19. 

3 Right precaval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal* vein. 
9 Trachea. 
10 Pulmonary artery. 
22 Vagus. 



FIGURES 136 AND 137 

136 Same, section 20. 

137 Same, section 21. 

3 Right i)recaval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Kxtraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 

6 Precardinal or precava of left side. 

7 Aorta. 

9 Trachea. 
10 l*ulmonary artery. 
22 Vagus. 



FIGURES 138 AND 139 

« 

13S Same, section 22. 
139 Same, section 23. 

• 

3 Right pre^aval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 P^xtraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein. 

6 Precardinal or precava of left side. 

7 .\orta. 

9 Trjichea. 
10 Pulmonarv arterv. 
22 Vagus. 



FIGURES 140 AND Ul 

140 Same, section 24. 

141 Same, section 25. 

3 Right precaval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing l3rmphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein. 

6 Precardinal or precava of left side. 



7 


Aorta. 


8 


Oesophagus. 


9 


Trachea. 


10 


Pulmonary artery. 


22 


Vagus. 



FIGUKES 142 AND 113 

142 Transverse section through ventral part of upper thoracic region in a 15 
mm. cat embr>'o (series 216, slide X. section 32), X 225. 

143 Same, section 33. 

3 Right precaval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 
5» Extrainthnal or perivenous lymphatic space surrounding degenerating embryonal vein. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 

10 Pulmonary artery. 
22 Vagus. 



FKJURKS 144 and 145 

144 Same, section 34. 

145 Same, section 35. 

3 Right prccaval vein. 

4 Atrophying embryonal vein, forming kernel in interior of devel
oping and replacing lymphatic space. 

5 Kxtraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein. 

6 Precardinal or precava of left side. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 

10 Pulmonarv arterv. 

18 Peritracheal venous plexus. 

22 Vagus. 



FIGURES 146 AND 147 

146 Transverse section through ventral part of upper thoracic region in 
a 15.6 mm. cat embryo (series 215, slide XIV, section 31), X 225. 

147 Transverse section through ventral portion of upper thoracic region in 
a 16 mm. cat embryo (series 230, slide XII, section 25), X 225. 

3 Right precaval vein. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 

6 Precardinal or precava of left side. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 

10 Pulmonary artery. 

22 Vagus. 

32 Ventral mediastinal venous plexus. 



FIGURE US 

148 Tninsvorso section through ventral portion of upper thoriicic region in 
a 16 mm. eat embryo (series 222, slide X, section 2), X 225. 

1 Sympathetic nerve. 

3 Right Azygos vein, thoracic porticm. 

() Precardinal or precava of left side. 

7 Aorta. 

8 Oesophagus. 
Trachea. 

10 Puhnonarv arterv. 

22 Vagus. 

3fi Thoracic duct, azygos segment. 

37 Hrnncho-mediastinal duct. 



FIGURES 149 AND 150 



149 Same, section 2. 

150 Same, section 3. 



FIGURES 151 AND 1.52 



151 Same, section 10. 

152 Same, section 15. 



FIGURE 153 

153 Same, section 16. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

6 Precardinal or prccava, resp. azygos of left side. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 

10 Pulmonary artery. 

22 Vagus. 

36 Thoracic duct, azygos segment. 

37 Broncho-mediastinal duct. 



FIGURKS lol AND lo2 



151 Same, section 10. 

152 Same, section 15. 



FIGURE 153 

153 Same, section 16. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

6 Precardinal or precava, reap, azygos of left side. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 

10 Puhnonary artery. 

22 Vagus. 

36 Thoracic duct, azygos segment. 

37 Broncho-mediastinal duct. 



FIGURE 154 

154 Transverse section through ventral portion of upper thoracic region in 
a 20 mm. cat embryo (series 241, slide, XIX, section 18). X 225. 

3 Right precaval vein. 

7 Aorta. 

8 Oesophagus. 

9 Trachea. 

10 Pulmonary artery. 

IS Peritracheal venous plexus. 

22 Vagus. 

37 Broncho-mediastinal duct. 



FIGURES 155 AND 156 



155 Same, section 19. 

156 Same, section 20. 

3 Right precaval vein. 

7 Aorta. 

9 Trachea. 

10 Pulmonary artery. 

22 Vagus. 

37 Broncho-mediastinal duct. 



FIGURES 157 AND 158 



157 Same, section 21. 

158 Same, section 22. 

9 Trachea. 

10 Pulmonary artery. 

22 Vagus. 

37 Broncho-mediastinal duct. 



DEVELOPMENT OF THE THORACIC DUCT 107 

B. The development of the proximal portion of the thoracic duct 
proper J between the termination of thoracic duct approach of the 
jugular lymph sac and the beginning of the azygos segment of the 
thoracic du^ts, caudal to the level of the aortic arch, viz, the preazygos segment of the thoracic duct. 

In the earlier purely venous stages a venous plexus between 
oesophagus and vertebral column (i7, fig. 101), drains caudolaterad into the mesal surface of the main jugular and innominate trunks. This plexus continues the supracardinal venous 
line cephalad beyond the level of the azygos-Cuvierian junction. The terminals of this plexus are frequently joined by 
dorsal somatic venous tributaries {16, fig. 101), near their entrance 
into the main vein. These vessels have been previously discussed 
in their relation to the general tributary system of thejuguloinnominate lin-e (cf. supra p. (92), and their disposition is schematically shown in fig. 101. 

In a 14 mm. embryo (series 210, slide viii, section 41, X 225) 
the dorso-medial or prevertebral tributary {17) and the dorsal 
somatic branch {16) are shown in fig. 102, just prior to their 
union into the common large trunk emptying into the dorsomedial angle of the internal jugular vein {25), dorsal to the sjinpathetic nerve (i). 

The same plexus elements {16 and 17) are seen in another 14 
mm. embryo (series 212, slide vii, section 23, X 150) in fig. 159. 
In this section their point of confluence and the entrance of the 
resulting combined trunk into the internal jugular vein takes 
place ventral to the sympathetic nerve (i), between the same 
and the left subclavian artery (55), by utilizing the pathway 
afforded by the peritracheal plexus {18, in fig. 102). 

Figs. 160 and 161 show these tributaries {16 and i7) in a 13.5 
mm. cat embryo (series 189, slide vii, sections 20 and 21) in a 
magnification of 225 diameters, as they are approaching their 
confluence and point of entrance into the internal jugular vein 
{25), In addition these sections afford admirable examples of 
two other conditions, previously noted (vide supra pp. 49) : 

a. The development of independent mesenchymal intercellular 
lymphatic spaces, with well defined endothelial limiting walls. 



108 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

Such spaces {77) are seen in the two sections lateral to the 
oesophagus. They apparently develop from the beginning as 
intercellular clefts, without relation to embryonic veins. The 
preazygos region presents these spaces in almost all 13 and 14 
mm. embryos. Their development in the mammalian embryo is 
of the utmost phylogenetic significance and affords important evidence in the interpretation of systemic lymphatic ontogenesis in 
the sauropsida, and especially in reptiles. The investigation of 
avian and reptilian lymphatic development has been carried on 
for the past year in the anatomical laboratory of Columbia University. These researches are now nearly completed, and some 
of the main results were presented at the 27th session of the 
American Association of Anatomists at Cornell University in 
December of last year. They establish a common genetic ground 
plan for the development and adult organization of the amniote 
lymphatic system. The avian and reptilian type only differs 
from that encountered in the mammal in respect to the higher 
degree of development of the jugular lymph sac, as an anterior 
or cervical veno-lymphatic heart, in the ontogenetic appearance 
of other areas of equal phylogenetic significance, as remnants of the 
multiple ancestral series of segmental veno-lymphatic hearts, 
and in the preponderance of peripheral lymphatic development 
by confluence of independent intercellular mesodermal spaces, 
not associated topographically, as in the mammal, with temporary embryonic venous channels. In other words, the extraintimal perivenous development of the majority of peripheral 
lymphatic channels described in this communication appears 
as a caenogenetic process in the mammalian embryo, whereas 
in the sauropsid amniotes most of the systemic lymphatic 
channels develop along more primitive phylogenetic lines, by the 
direct confluence of numerous intercellular mesodermal spaces. 

These relative conditions have been outlined in a previous 
publication on the phylogenetic relations of the lymphatic and 
blood-vascular systems in vertebrates.*^^ The results of the more 

*■ Geo. S. Huntington, "The phylogenetic relations of the lymphatic and 
blood -vascular systems in vertebrates.*' 
Anat. Record, vol. IV, no. 1, January 1910. 



DEVELOPMENT OF THE THORACIC DUCT 109 

recent detailed investigations of Ijonphatic development in birds 
and reptiles have fully sustained the interpretation given in the 
publication quoted. 

b. The darkly stained mass of cells seen in the interval between 
16 and i7 in both sections is the result of obliteration of early 
embrj^onic vascular channels, which have lost their connection 
with the vessels, and whose endotheUal walls are apparently in 
the process of reverting to indifferent mesodermal cells. Many 
of these degenerated vascular aggregations are formed in embryos 
between 13 and 15 mm. crown-rump measure. 

Some of the elements of this early embryonic prevertebral 
venous plexus are secondarily replaced by perivenous or extraintimal IjTnphatic spaces in exactly the same way as is observed in 
the development of the ventral mediastinal duct. The resulting, 
originally separate, extraintimal lymphatic anlages, having replaced the venule along and around which they primarily developed, unite with each other and form the preazygos segment 
of the thoracic duct, between the thoracic duct approach of the 
jugular lymph sac and the level of the aortic arch, at which the 
azygos portion of the thoracic duct begins. 

Fig. 162 shows a transverse section of the left side of the upper 
thoracic region in a 14 nron. cat embr^^o (series 210, slide IX, 
section 26, X 200). The prevertebral tributarj^ plexus (17) turns 
mesad of the sympathetic nerve (1) to enter the dorso-medial 
angle of the left innominate vein (40), Dorsad of the main vein 
is the ascending portion of the left subclavian artery (S3). Between aorta (7) and innominate vein (40) are other elements of 
the mediastinal venous plexus, in the interval between the sympathetic nerve (1) and the vagus {22) j with ventral branches (32) in 
front of the latter. 

Between the oesophagus and the prevertebral plexus (17) is 
an area in which venous elements (4), formerly connected with 
the same, are undergoing replacement by the extraintimal lymphatic anlages (5) of the preazygos segment of the thoracic duct. 
These structures cannot be distinctly made out in fig. 162, but 
they are shown in a higher magnification in detail in fig. 163, 
which includes the region of the same section dorsal to the oesoph


110 DEVELOPMENT OP THE SYSTEMIC LYMPHATIC VESSELS 

agus magnified 225 diameters. The prevertebral venous plexus 
(17) extends in an arch concentric with the dorsal circumference 
of the oesophagus (5), in front of the vertebral centers. Between 
it and the oesophagus, mesal to the sympathetics (i), are seen 
on each side former elements of the venous plexus (4) surrounded 
by the extraintimal lymphatic anlages (5) of the preazygos segment of the thoracic duct. 

Figs. 164, 165 aiid 166 show the same structures in the next 
three sections (25, 24 and 23), proceeding cephalad. Fig. 166 
is especially clear. In it the original line of connection of the 
atrophying venous kernel (4) with the prevertebral plexus (17) 
can still be made out as a band of condensed mesoderm, and 
the endothelium of the perivenous lymphatic space (5) is clearly 
marked. 

Figs. 167 and 168 show this area in two successive sections of 
the same embryo further caudad (series 210, slide ix, sections 
43 and 44, X 150), and fig. 169 gives the last section magnified 
200 diameters. The empty central venous remnant (4), with 
the enveloping extraintimal lymphatic anlage (5), and the still 
functional elements of the prevertebral plexus (17), can be seen 
in all of the sections. They also show, nearer to the dorsolateral wall of the oesophagus, one of the collections of darkly 
stained mesodermal cells above referred to as representing remnants of formerly patent blood-vessels. 

The series of microphotographs shown in figs. 160 to 169 
inclusive again conclusively demonstrates the origin of this 
portion of the lymphatic channel by confluence of independent 
extraintimal mesenchymal spaces surrounding and replacing 
degenerating embryonic venules. The reproductions only give 
relatively faint and indistinct views of the actual conditions observed under the microscope. The general mesenchymal tissue 
in this region is extremely loose and the area is very difficult 
to photograph sharply and distinctly. The actual sections, 
however, offer histological pictures identical with those observed 
as above described in the development of the ventral mediastinal 
lymphatic duct. The extraintimal lymphatic spaces are either 
closely applied to part of the circumference of the wall of the 



DEVELOPMENT OF THE THORACIC DUCT 111 

shrinking venule, or they occasionally completely surround the 
same. In the former case the contained venous remnant is 
connected at part of its periphery with the wall of the enveloping lymphatic space. In the latter and more exceptional case, 
the free ventral nucleus of the lymphatic space is formed by the 
atrophied vein. In either case the lumen of the' latter may contain a few degenerated red blood cells. These pictures are again 
constant in embryos of the appropriate stages. The lymphatic 
anlage can be accurately traced from its indefinite beginning 
among the perivenous mesenchymal intercellular clefts through 
a number of successive sections to its similar distal terminations 
in the same intercellular plexus. Following the sections from 
this point caudad through a varying intervening area in which 
no distinct lymphatic channel appears, the same line will sooner 
or later reveal the repetition of the same process, and the formation 
of another link in the still disjointed chain of primitive lymphatic 
aniages. 
It is again to be noted here that in the earlier stages (13, 13.5, 

14 mm.), the mdividual spaces, plus thek kernel of atrophied 
vein, are relatively larger than in the later (15-15.5 mm.) embryos. In the earlier stages (13 nrni., 13.5 mm. and 14 mm. 
embryos) these separate and still isolated segments of the future 
continuous lymphatic channel begin and end blindly. In the 

15 and 15.5 mm. stages they have increased in number and adjacent links have united to form longer segments. Finally, in 
the 16 mm. cat embryo, the preazygos portion of the thoracic 
duct is usually established as a nearly continuous channel through 
the further confluence of the originally separate and distinct 
components. Every stage of the extraintimal lymphatic development can be observed with absolute certainty and accuracy in 
every series within the proper length limits. 



FIGURE 159 

159 Transection of upper thoracic region in a 14 mm. cat embryo (series 212, 
slide VII, section 23), X 150. 



1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

11 Jugular lymph sac. 

16 Dorso-medial somatic venous tributaries. 

17 Prevertebral venous plexus. 

20 Subthymic venous plexus. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 
25 Internal jugular vein. 
33 Left subclavian artery. 



PART II, PLATES 

FIC;URES 159 TO 169 



FIGURE 159 

159 Transection of upper thoracic region in a 14 mm. cat embryo (series 212, 
slide VII, section 23), X 150. 



1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

11 Jugular lymph sac. 

16 Dorso-medial somatic venous tributaries. 

17 Prevertebral venous plexus. 

20 Subthymic venous plexus. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 
25 Internal jugular vein. 
33 Left subclavian artery. 



FIGURES 162 AND 163 

162 Transverse section of upper thoracic region in a 14 mm. cat embryo 
(series 210, slide IX, section 26), X 200. 

163 Dorsal portion of same section, X 226. 

1 Sympathetic nerve. 

4 Atrophying embryonal vein, forming kernel in interior of develop
ing and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein. 

7 Aorta. 

17 Prevertebral venous plexus. 

22 Vagus. 

32 Ventral mediastinal venous plexus^ 

33 Left subclavian artery. 
40 Innominate vein. 



FIGURES 162 AND 163 

162 Transverse section of upper thoracic region in a 14 ram. cat embryo 
(series 210. slide IX, section 26), X 200. 

163 Dorsal portion of same section, X 225. 

1 Sympathetic nerve. 

4 Atrophying embryonal vein, forming kernel in interior of developing and replacing lymphatic space, 
o Kxtraintimal or perivenous lymphatic space surrounding degenerating embryonal vein. 
7 Aorta. 

17 Prevertebral venous plexus. 
22 Vagus. 

32 Ventral mediastinal venous plexus* 

33 Left subclavian arterv. 
40 Innominate vein. 



FKIUHES im, 165 AND \m 

164 Same, section 25. 

165 Same, section 24. 

166 Same, section 2ii. 

1 Sympathetic nerve. 

4 Atrophying embryonal vein, fonniug kernel in interior of develop
ing and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic apace surrounding <iegen
crating embryonal vein. 
8 Oesophagus. 
17 Prevertebral venous plexus. 



FIGURES 167 AND 168 

167 Same, section 43 X 150. 

168 Same, section 44 X 150. 

1 Sympathetic nerve. 

4 Atrophying embryonal vein, forming kernel in interior of develop
ing and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein, 
17 Prevertebral venous plexus. 



FIGURE m) 
169 Same, section 44. X 200. 

1 Sympathetic nerve. 

4 Atrophying embryonal vein, forming kernel in interior of develop
ing and replacing lymphatic space. 

5 Kxtraintimal or perivenous lymphatic space surroumiing degener
ating embryonal vein. 
8 Oesophagus. 
40 Innominate vein. 



•J 



FIGURE 170 

170 Reconstruction of left vascular complex of lower cervical and upper 
thoracic regions of a 15 mm. cat embryo (series 218, slide VIII, sections 25 to 
44; slide IX, sections 1 to 48; slide X, sections 1 to 48; slide XI, sections 1 to 
48; slide XII, sections 1 to 48, X 225), dorsal view. 

1 Sympathetic nerve. 

3' Right azygos vein. 

3 Right precava. 

6 Left precava. 

6' Left azygos vein, thoracic portion. 

7 Aorta. 

10 Pulmonary artery. 

12 Jugular lymph sac, thoracic duct approach. 

16 Dorso-medial somatic venous tributaries. 

22 Vagus. 

24 Thyrocervical artery. 

33 Left subclavian artery. 

35 Thoracic duct, preazygos segment. 

35' Detached lymphatic space in path of preazygos channel. 

37 Broncho-mediastinal duct. 

41 Vertebral artery. 

42 Vertebral vein. 

45 Innominate artery. 

46 Left superior intercostal vein. 

53 Precaval lymphatics. 

54 Fifth spinal nerve. 

55 Sixth, seventh and eighth spinal nervt 

56 Ductus arteriosus Hotalli. 

57 Right subclavian artery. 



FIGURE 171 

171 Reconstruction of left vascular complex of lower cervical and upper thoracic 
regions in a 15.5 mm. cat embryo, (series 143, slides VIII, IX, X, and XI), X 225 
View from behind and from right side. 

1 Sympathetic nerve. 
3' Right azygoB arch. 
3 Right precava. 

6 Left precava. 

6' Left azygos vein, thoracic portion. 

7 Aorta. 

12 Jugular lymph sac, thoracic duct approach. 

13 Jugular lymph sac, jugular approach. 
17 Prevertebral venous plexus. 

19 Suprathymic venous plexus. 

20 Subthymic venous plexus. 

21 Thymus. 

22 Vagus. 

23 Left carotid artery. 
23' Right carotid artery. 

24 Thyrocervical artery. 

29 Jugulo-subclavian trunk. 

35 Thoracic duct, preazygos segment. 

36 Thoracic duct, azygos segment. 

40 Innominate vein. 

41 Vertebral artery. 

42 Vertebral vein. 

45 Innominate artery. 

54 Fifth spinal nerve. 

55 Sixth, seventh and eighth spinal nerve 
57 Right subclavian artery. 



FIGURES 172 AND 173 

172 Traiiaverso section of loft side of upper thoracic rej^iori of a 15 mm. 
cat embryo, (series 143, slide XI, section 10), X 2(K). 

173 Same, section 14. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

17 Prevertebral venous plexus. 

33 Left subclavian arterv. 

35 Thoracic duct, ])reazygos segment. 

37 Broncho-mediastinal duct. 

38 Confluence of broncho-mediastinal duct and prcazygos segment of 

thoracic duct. 
40 Innominate vein. 



KIGUKKS 174. 175 AND 176 

174 Same, section 12. 

175 Same, section 11. 

176 Same, section 6. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

33 Left subclavian artery. 

35 Thoracic duct, preazygos segment. 

37 Broncho-mediastinal duct. 

38 Confluence of broncho-mediastinal duct and preazygos segment of 

thoracic duct. 
40 Innominate vein. 



FIGURES 177, 178 AND 179 

177 Same, section 5. 

178 Same, section 2. 

179 Same, slide IX, seetion 32. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

35 Thoracic duct, prcazygos sej^ineni. 

37 Bron(!ho-mediaatinal duct. 

38 Confluence of broncho-mcdiastinal (hict and preazvRos sei^eni <»f 

thoracic (hict. 

40 Innominate vein. 

41 Vertebral arterv. 
44 (\)sto-rervical vein. 



FICiURKS ISO, 181 A\D 182 

ISO Same, slide X, section 28. 
181 Same, slide X, section 20. 
1S2 Same, slide X, section 23. 

1 Sympathetic nc^-ve. 

8 Oesophagus. 

9 Trachea. 

33 Left subclavian artery. 

38 Confluence of l)roncho-inediastinal duct and preazygos segment of 
thoracic duct. 

40 Innominate vein. 

41 \'ertel)ral artery. 

43 ('o<to-cervical arterv. 

44 (\)sto-c(M*vical vein. 



FIGURE 183 
183 Same, slide X, section 22. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

12 Jugular lymph sac, thoracic duct approach. 

22 Vagus. 

23 Left carotid artery. 

33 Left subclavian artery. 

35 Thoracic duct, preazygos segment. 

40 Innominate vein. 

41 Vertebral artery. 

43 Costo-cervical artery. 

45 Innominate artery. 



FIGURES 184 AND 185 

184 Transverse section through upper part of left thoraric region in a 
15.5 mm. cat embryo, (series 141. slide X, section IS), X 200. 

185 Same, section 21. 

1 Sympathetic nerve. 

8 Oesophagus. 

9 Trachea. 

16 Dor.so-medial somatic venous tributaries. 

18 Peritracheal venous plexus. 

22 Vagus. 

23 Left carotid artery. 

33 Left subclavian artery. 

38 Confluence of broncho-niediastinal duct and preazygos segment of 

thoracic duct. 
40 Innominate vein. 



FIGURE 18S 

188 Reconstruction of cephalic portions of azygos veins and anlages of 
azygos segment of thoracic ducts in a 13.5 mm. cat embryo, (series 76, slide X, 
sections 1 to 27; slide XI, sections 1 to 38; slide XII, sections 1 to 40; slide XIII. 
sections 1 to 33; slide XIV, sections 1 to 7) , X 225. Ventral view. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

6 Left azygos vein, thoracic portion. 



FKJURK 189 

189 Reconstruction of cephalic portions of azygos veins and anlages of 
azygos segment of thoracic ducts in a 14 mm. cat embryo; series 34 (Princeton 
Embryological (Collection), slides XXIV to XXXTI, 222 sections, X 225. Ventral 
view. 

1 Sympathetic nerve. 
3 Right precava. 

3' Right azygos vein, tlioracio portion. 
6 Left precava. 

6' Left azygos vein, thoracic portion. 
34 Ventro-medial azygos plexus. 



FIGURE 190 

190 Reconstruction of cephalic portion of azygos veins and anlages of azygos 
segment of thoracic ducts in a 14 mm. cat embryo; (series 214, slides XIII, XIV, 
XV, XVI and XVII i, X 225. Ventral view. 

1 Sympathetic nerve. 
3 Precardinal or precava of right side. 
3' Right azygos vein, thoracic portion. 
6 Precardinal or precava of left side. 
6' Left azygos vein thoracic portion. 
34 Ventro medial azygos plexus. 



FIGURE 19() 

100 Roconstriiction of (•e[)hiilic portion of azygos veins and milages of azygos 
segment of thoracic duets in a 14 mm. cat embryo; (series 214. slides XIII, XIV, 
XV, XVI and XVII ), X 22.'). Ventral view. 

1 Sympathetic nerve. 

3 Precardinal or precava of right side. 

3' Right azygos vein, tlioracic portion. 

6 Precardinal or i)recava of left side, 

f)' Left azygos vein thoracic portion. 

34 Ventro medial azygos ple.xus. 



FIGURE 191 

191 Ucoonstnirtion of cephalic portions of azygon veins and aniages of 
azygoH segment of thoracic ducts in a 15 mm. cat embryo; (series 219, slides 
XTV, XV, XVI and XVII), X 225. Ventral view. 

1 Sympathetic nerve. 



FIGURE 192 

192 Reconstruction of cephalic portions of azygos veins and anlages of 
azygos segment of thoracic ducts in a 15.5 mm. cat embryo; (series 143, slides 
XIV, XV, XVI, XVII and XVTII) X 225. Ventral view. 

34 Ventro-medial azygos plexus. 



FIGURK 193 

193 Reconstruction of azygos veins and of thoracic and right lymphatic ducts 
In a 16 mm cat ombrvo: ('serios96, slides VII to XVI) X 225. Ventral view. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

6 Left azygos vein, thoracic portion. 

47 Right lymphatic duct. 

51 Mesenteric lymphatics. 



138 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

(f)) is larger and still contains a number of red blood cells. In the 
four succeeding sections, 19, 20, 21 and 22 (figs. 248, 249, 250 and 
251) the former line of communication of the decadent venule (4) 
with the functional azygos channel can still be distinctly traced as 
a strand of connective tissue cells joining it to the beginning of the 
right interazygos plexus. The separation of the venous radicle 
undergoing extraintimal lymphatic replacement has just been 
accomplished in this area. 

The six sections of this embryo shown in figs. 246 to 251 should 
he compared with the slightly more advanced 14 mm. embryo 214; 
where, e.g., in figs. 230, 231, 232, 214, 215, 216, 217, 218 and 219 
exactly equivalent sections are given, showing the next step in extraintimal lymphatic development in this region. The atrophying 
venule (4) in the earlier embryo (series 34) still contains red 
blood cells and still betrays its original connection with the functional venous channels. In the genetically slightly older embryo 
(series 214) the same structure appears now as an empty endothelial bag (4), completely detached from the azygos veins. In both 
embryos this decadent venous radicle is surrounded by the developing extraintimal lymphatic space (5). The comparison of 
the sections shows every step in the process of development in 
these two closely connected stages. The reduced photographic 
reproductions do not give the clear and unmistakable pictures 
presented by the actual sections, owing to the loss of the diflFerential stain and of the focal adjustment. Still the contour of the 
venous core, undergoing atrophy and replacement by the extraintimal lymphatic anlage, its content of red blood cells and its 
recently interrupted connection with the main azygos vein in the 
younger embryo (series 34), can be followed with a sufficient degree 
of clearness and can be contrasted with the conditions presented 
by the succeeding stage (series 214). 

Figs. 244 and 245 give two successive sections from the caudal 
part of the thoracic region in series 34 (slide xxxi, sections 18 
and 19, X 225) in which the earlier conditions, preceding the first 
appearance of the lymphatic anlages of the thoracic duct in the 
azygos segment, are shown. 

Between the right azygos vein {3) and the aorta (7) are seen 



DEVELOPMENT OF THE THORACIC DUCT 139 

the components of the ventro-medial azygos plexus {4)f partially 
separated from the main venous trunks, but not, as yet, surrounded by extraintimal lymphatic anlages, as, further cephalad, 
'(slide xxviii) in the sections just described, (figs. 246 to 251). 

The 15 mm. and 15.5 mm. embryos show, in the majority of 
instances, an advance over the preceding stage in two directions : 

I. The central venous core of the 14 mm. embryo is further 
reduced or entirely eliminated, leaving the lymphatic anlage, 
which formerly surrounded it, with a clear lumen. 

II. The individual scattered lymphatic areas have united to 
form longer segments of the future lymphatic channel system. 
This condition is well shown in the ventral view of the reconstruction of an average 15 mm. embryo (series 219) in fig. .191 (cf. 
supra, p. 126). 

Figs. 252 to 258 inclusive show transverse sections of the lower 
thoracic region in a 15.5 mm. cat embryo, (series 143, slide xviii 
section 7, 11, 12, 13, 14; slide xvii, sections 31 and 32, X 225), 
and fig. 192 gives the ventral view of the reconstruction of the 
azygos region in this embryo, comprising slides xiv, xv, xvi, 
xvii, and xviii. 

The sections (figs. 252 to 258) show the following changes in the 
vascular structures, compared with the preceding stages 

I. The right (S) and left (6) azygos veins are concentrated, 
more sharply defined and relatively smaller, although still equally 
developed on both sides. 

II. The interazygos anastomosis is still well developed and 
uniform (cf. also fig. 192). 

III. The entire azygos complex is much more closely apphed 
to the dorsal and dorso-lateral circumference of the aorta (7), 
resulting in the practical obliteration of the interval between the 
main veins and the artery seen in the preceding stages. 

IV. This topographical rearrangement has forced the ventromedial azygos tributaries, where they still persist {34 in figs. 252, 
253, 257), and the thoracic duct imlage (36) to pass from the 
ventro-medial to the ventral aspect of the main azygos trunks. 

V. Both azygos veins lie in the region ventro-lcUeral to the intersegmental arteries. The supra-aortic area between them is still 



140 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

occupied by the interazygos (supra-cardinal) anastomosis (cf. 
infra, figs. 261 and 262). 

VI. The sections taken from the caudal portion of the thoracic 
region (slides xvii and xviii) show the right and left thoracic 
duct anlages (36) following the ventral aspect of the respective 
azygos veins (cf. fig. 192). They are not yet united into a continuous channel, but their lumen is clear, without trace of the venous 
kernel around which they developed. 

Fig. 252 (slide xviii, section 7) shows renmants of the ventromedial azygos plexus (34) emptying on both sides into the azygos trunks. Lateral to these venous radicles lies the thoracic 
duct anlage of each side {36) . 

In section 11 of the same slide (fig. 253) the right thoracic 
duct anlage has enlarged and presents a beautifully clear picture 
of the relation of this structure to the rightazygos vein at this stage. 

On the left side the conditions are as in the preceding figure, 
both persistent ventral venous tributary (34) and left thoracic duct 
anlage (36) lying side by side. 

In the two succeeding sections, 12 and 13, (figs. 254 and 255) the 
right thoracic duct continues well developed and presents a 
pointed dorso-mesal prolongation indicative of its situation in the 
earlier stages, on the mesal aspect of the vein, between it and the 
aorta, and ventral to the interazygos anastomosis, (cf. series 
34 and 214). The left duct anlage continues as a small channel. 

In section 18, (fig. 256) both right and left lymphatic anlages 
cease as distinct chaimels, marking one of the intervals between 
the still disconnected segments of the future continuous duct. 

Figs. 257 and 258 (sections 31 and 32 of slide xvii) show on 
alternating sides small thoracic duct anlages (36), and in the root 
of the dorsal mesogastrium sections of the well-developed anterior 
mesenteric lymphatics (61). Some of the later stages (series 253, 
figs. 265 to 270) will show the full development of these mesenteric channels and their confluence with the thoracic duct. 
Tliis area, is, however, responsible for the development of what 
I have above defined as the post-azygos segment of the thoracic 
duct and will hence be considered in detail in the second volume 
of this series. 



DEVELOPMENT OF THE THORACIC DUCT 141 

In comparison with the series just considered figs. 259 and 
260 show transverse sections of the lower thoracic region of series 
258, slide xviii, sections 1 and 9, X 225. This embryo is rated 
as 17 mm. in crown-rump length, but the lymphatic development of the azygos region Ls relatively retarded and only slightly 
in advance of the conditions presented by the 15.5 mm, series 
143. Direct comparison of figs. 252 to 258 with figs. 259 and 
260 will show this correspondence, both at the lev^l of the intersegmental arteries {2 in fig. 260), and in the intervals between them 
(fig. 259) . In the older embrj'^o the right and left thoracic duct anlages (36) are somewhat larger and form longer channel segments, 
but otherwise the two series belong practically to the same developmental stage, in spite of their difference in total length measure. 
The correspondence, for example, between figs. 254 (series 143) 
and 259 (series 258) is remarkable. 

On the other hand the majority of 16 mm., 16.5 mm. and 17 mm. 
embryos offer decided advances in the lymphatic development of 
this region beyond that normally found in the 15 mm. and 15.5 
mm. stages. 

Two successive sections of a typical 16 mm. embryo (series 96) 
in the azygos area are shown in figs. 261 and 262, and fig. 193 
gives the ventral view of the reconstruction of the same embryo, 
in which the level of figs. 261 and 262 is indicated by the line A-B. 

Comparison with the immediately preceding series (143 and 
258) will show that the following fundamental changes have occurred in the azygos venous and lymphatic systems : 

I. The two azygos veins (S and 6) have become reduced in size. 
At the level, at which the sections of figs. 261 and 262 are taken, 
both veins now lie dorsal to the intercostal arteries (2), whereas in 
the earlier stages (e.g. figs. 260, 258, 257) the azygos trunks are 
ventral to the arteries, and the interval between the latter, along the 
dorsal aspect of the aorta, is occupied by the supracardinal interazygos plexus. 

Reference to the reconstruction of series 96 (fig. 193) 
shows that this topographical readjustment has occurred in the 
caudal part of the azygos area, below the level A-B, by the longitudinal hydrostatic definition of the main supracardinal azygos 



142 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

trunks through confluence of elements of the preceding interazygos plexus. The original post-cardinal azygos veins, which in 
series 258 and 143 are seen to form the main channels ventral to 
the intercostal arteries, are, in the caudal region of series 96, 
represented by two slender longitudinal trunks, on the lateral 
aspect of the thoracic ducts between them and the sympathetic 
nerves (1). The main azygos veins have developed as distinct 
circumscribed axial chaimels out of the antecedent supracardinal 
interazygos plexus, dorsal to the intercostal arterial branches (S) . 
Correlated with this new azygos development is the reduction of 
the earlier postcardinal channels, ventral to the intersegmental 
arteries, and their topographical replacement in large part by the 
right and left thoracic ducts {36) (not labelled in fig. 193). 
Cephalad of the level A-B the reconstruction shows the earlier 
relation of the azygos trunks, ventro-lateral to the intercostal 
arteries. In ascending the left azygos vein gradually diminishes, 
while conversely the vessel of the right side increases in caliber. 

II. The individual separate lymphatic anlages of the azygos 
segment of the thoracic duct of the preceding stages have united 
into a continuous and uninterrupted lymphatic channel. 

Caudad of the level A-B (fig. 193) the right and left thoracic 
ducts are fairly symmetrical bilateral channels, connected with 
each other by several broad and by a larger number of slender 
transverse anastomoses. They occupy the position of the earlier 
postcardinal azygos trunks, before these shifted to the supracardinal position, ventro-lateral to the intercostal arteries, along 
the medial border of the reduced longitudinal tributary channel 
representing on each side the remnant of the earlier post-cardinal 
azygos, and draining dorsad into the newly established supracardinal azygos line of each side. 

Figs. 261 and 262 give excellent views of the topographical 
relations of the vascular structures, arterial, venous and lymphatic. Both sections show the right and left thoracic ducts (36), 
ventral to the intercostal arteries (2), the lymphatic cross anastomosis between the two along the dorsal circumference of the 
aorta, and the main supracardinal azygos veins (5, 6) . Cephalad 
of the level A-B (fig. 193) this plexiform anastomosis between the 



DEVELOPMENT OP THE THORACIC DUCT 143 

ducts increases in extent, and the entire lymphatic channel inclines, in ascending, to the left. This, as previously explained 
(cf. supra, p. 129), is due to the greater development of the intermediate lymphatic line, along the ventral aspect of the interazygos 
anastomosis, and its union with the left thoracic duct to form the 
plexiform channel of the adult. The corresponding lymphatic 
of the right side, on the other hand, becomes reduced above the 
level A-B, and only its cephalic portion persists as the thoracic 
segment of the right lymphatic duct (47 in fig. 193). 

The extraintimal lymphatic anlages ventral to the thoracic 
ducts, which are eventually to establish the coimection between 
them and the mesenteric lymphatics, are in the process of development in series 96. The venous core (4) and the replacing perivenous lymphatic (5) are shown on the left side in figs. 261 and 
262, and equivalent segments of this channel are seen in the reconstruction {61 in fig. 193). In other portions of the ventral and 
ventro-lateral periaortic mesoderm numerous independent intercellular spaces begonging to the same system are developing. 

While the thoracic ducts are in the majority of 16 mm. embryos 
complete continuous and definite channels, as in the present average example, the acquisition of this final condition is not infrequently delayed considerably beyond this period. I have a number 
of 16 and 16.5 nmi. embryos in which the thoracic duct development has not advanced beyond the stage typical of the average 
14 mm. or 15 nmi. embryo. This is another example of the considerable range of chronological variation of lymphatic development in individual embryos encountered in examining a large 
number of series of about the same length measure. 

The 16 mm. embryo again furnishes conclusive evidence as to 
the secondary character of the mutual relation between embryonic 
venous and lymphatic vessels, and shows, in typical individuals, 
the final stage of the process through which temporary venous, 
channels are replaced by the permanent components of the lymphatic system. This replacement, as demonstrated by the successive series of sections from the azygos region just considered, is 
a gradual process. The lymphatic channel has its inception in 
numerous small extraintimal mesenchymal spaces which form 



144 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

along and around the components of an atrophying embryonic 
venous plexus, or follow part of the circumference of a more definite 
early venous trunk. As these spaces increase, enlarge and become 
confluent to form longer segments of the lymphatic channel, the 
related venous element continues to recede, imtil, in certain areas, 
it is entirely replaced by the lymphatic vessel. In other districts, 
along embryonic veins which are carried into the adult organization, as permanent components of the venous system, the redundant vein of the earlier stages becomes more circumscribed and 
more clearly defined as the companion lymphatic channel develops 
in the perivenous area. In either case the complete or partial 
replacement of venous by lymphatic elements does not occur 
suddenly, but is accomplished by gradual and progressive ontogenetic stages. I can find no evidence at any point of the separation of portions of a venous plexus or of an already organized 
venous chaimel, such detached parts then uniting directly with 
each other to form systemic lymphatic vessels. In every region 
of the mammalian embryo the above described extraintimal 
development of the lymphatic elements, and the subsequent 
secondary topographical replacement of decadent veins by them, 
can clearly be demonstrated. This process, of course, leads to a 
stage in which the advancing development of the lymphatic and 
the correlated regression of the associated venous components 
are balanced, and in which both, proceeding in opposite genetic 
directions, are foimd side by side in the same field. The stages 
previously discussed in detail, between 13 mm. and 15 mm. offer 
abundant illustration of this intermediate stage in the azygos 
area. 

It is to be noted that in the earlier stages (13 to 14 mm.) the 
lymphatic extraintimal spaces first appear on the lateral aspect 
of the atrophying venules of the ventro-medial azygos plexus, and 
subsequently surround them. They are then situated at some 
distance ventral to the main azygos trunks. In the later stages 
(15 mm., 15.5 mm. and 16 mm. embrj'os) they have extended 
dorsad and lie in close apposition to the ventral and ventro-medial 
circumference of the larger veins, which position they maintain 
subsequently in their further development. Coincident with this 



DEVELOPMENT OF THE THORACIC DUCT 145 

relative change in position of the earlier lymphatic spaces is the 
appearance of additional thoracic duct anlages, which develop 
as extraintimal lymphatic elements along those lines of the embryonic azygos system which are destined to undergo, in the 
later stages, still further reduction and final elimination in the 
definite organization of the adult condition. [Compare on this 
point the sections of series 96 (figs. 261 and 262) with those of 
series 253 (figs. 265 to 270)]. 

One other fact deserves careful consideration in analyzing the 
development of the azygos segment of the thoracic ducts in stages 
between 14 mm. and 15 mm. In a certain proportion of the embryos of this period the extraintimal replacement of the earlier 
ventro-medial azygos plexus in the cephalic part of the future 
azygos segment of the thoracic duct is delayed. In these cases 
peculiar histological pictures are obtained in this area. The components of the ventro-medial azygos plexus have become detached 
from the main veins, and have fused together into an elongated 
spindle shaped bag, completely filled with blood, beginning and 
ending blindly and not in commimication with any venous channel. 
This structure, when found, invariably occupies the site of the 
long lymphatic segment seen m the reconstruction of series 214 
(fig. 190) on the right side, in the areas A and B (slides xiv and 
xv), ventral to the right intercostal arteries, in the interval 
between aorta and right azygos vein. The appearance presented 
by it on section is shown in figs. 263 and 264 in a 14 mm. cat 
embryo (series 211, slide xii, sections 2 and 8, X 225). It is 
indicated in these figures by the leader 5^, as a detached and confluent part of the original ventro-medial azygos plexus. Fig. 263 
shows this structure in the interval between the intercostal arteries. Fig. 264 gives a typical view of it at the level of one of the 
right intercostal branches. It lies ventral to the same, between 
aorta (7) mesad, the right azygos trunk (5) laterad, dorsal to the 
oesophagus (5). The blood cells, which completely fill its lumen, 
diflferentiate from those circulating in the continuous vein channels 
by remarkably intense reaction to the Orange-G stain. As 
stated, this structure is completely detached from all adjacent 
veins, can be followed cephalad and caudad through many sec


146 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

tions, and ends blindly at either end in a gradually diminishing 
pointed extremity. In a reconstruction of this embryo it would 
correspond absolutely in extent and relations to the long lymphatic channel above referred to on the right side of series 214 
(fig. 190). A comparison of the reconstruction (fig. 190) and of the 
corresponding sections (figs. 214 to 240) of this latter embryo, 
clearly reveal the significance of this, at first sight, somewhat 
anomalous and puzzling structure. It will be noted that the reconstruction of series 214 (fig. 190) shows, at the level of the line C, 
the caudal end of a large ventro-medial tributary trunk {34) of 
the right azygos vein (S), which, in proceeding cephalad, becomes 
imbedded in the centre of the long extraintimal Isrmphatic channel. The continuation of this venous tributary line, detached 
from the functional veins, furnishes the central venous core (4) 
which is surrounded by the extraintimal lymphatic space (6) in 
all the sections of series 214 shown in figs. 214 to 240 inclusive. 
If this ventro-medial tributary trunk {34 in fig. 190) had organized 
in its entire length, by confluence of the radicles of the preceding 
plexus, and had then become detached from the fimctional right 
azygos vein, it would, before extraintimal development of the 
surrounding lymphatic spaces began, present exactly the conditions seen in series 211. In comparing, therefore, these two 14 
mm. embryos, we find in series 214 the venous line, around which 
this important segment of the thoracic duct develops and which it 
subsequently replaces, present in the condition typical for the 
average embryo of this period, as a detached and nearly empty 
venous bag, surrounded by the extraintimal lymphatic channel. 
On the other hand, series 211 shows the same tributary trunk, also 
detached from the main vein, but still filled with blood, while the 
enveloping extraintimal lymphatic anlages have not yet made 
their appearance. Comparison with the reconstruction and with 
the sections of series 214 prove its identity with the latter's venous 
core (4) in the interior of the lymphatic channel (5). 

A 15 mm. embryo of the Princeton embrj^ological collection 
(series 53), which I had the opportunity of studying through the 
courtesy of Professor McClure, shows conditions identical with 
those just described in series 211. It is interesting and conclusive 



DEVELOPMENT OF THE THORACIC DUCT 147 

to further compare in this respect the reconstruction of series 
214 (14 mm. fig. 190) with that of series 143 (15.5 mm. fig. 192). 
In the former embryo the secondary para-azygos channel of the 
right side (34), developed by confluence of components of the 
right ventro-medial azygos plexus, only persists in its caudal 
portion, and has in the rest of its original extent been detached and 
surrounded by the extraintimal lymphatic channel. On the other 
hand, in the 15.5 mm. series 143 (fig. 192) this normal process of 
detachment and replacement by extraintimal lymphatic anlages 
has been delayed. Fig. 192 shows the para-azygos ventro-medial 
channel (34) as an extensive tributary trunk of the right azygos 
vein, cephalad of the level C. Only a few areas of the extraintimal lymphatic development occur, as yet, along its course. Further development of these and their confluence will produce the 
condition already seen in the earlier embryo, series 214, which is 
typical for the average embryo of the 14 mm. stage. Thus 
unusual and atypical delay of lymphatic development occurs in 
some embryos of this period in the region above specified, and produces a definite and uniform aberrant picture. The correct 
interpretation of the same is given by the conditions obtaining in 
the average embryo of this period. I lay some stress on the facts 
just described, because isolated observation of an instance of this 
character might readily lead to the erroneous assumption that the 
detached venous bag (34) of figs. 263 and 264 became directly 
transformed into the lymphatic channel of the thoracic duct occupying in the later stages the identical topographical position and 
maintaining the same relations to surrounding structures. This 
error can only be avoided by determining, in numerous embryos 
of this period, the typical and average condition of lymphatic 
development. 

Thus in the average 16 mm. cat embryo the originally separate 
and independent extraintimal anlages of the two thoracic ducts 
have become confluent, and form from this stage onward usually 
a continuous and uninterrupted lymphatic channel, which is connected with the general venous system through the jugular lymph 
sac, by union with the thoracic duct approach of the latter. 

From this stage forward the subsequent growth and readjust


148 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

ment of the thoracic ducts is merely a question of continuous 
enlargement of the lymphatic channels at the eicpense of the azygos veins. The latter recede still further, while the former correspondingly increase until the adult relative condition of both 
systems is attained. In this readjustment the thoracic ducts 
of the adult cat acquire for themselves in large part the topographical position occupied in earlier embryonic stages by portions of the azygos complex. The method of this substitution has 
been sufficiently and repeatedly detailed in the preceding pages. 

Figs. 265 to 270 inclusive show the results in transverse sections 
of the middle thoracic region m a 19 mm. cat embryo (series 253, 
slide xxiv, sections 9, 11, 15, 16, 17 and 18, X 225). 

In fig. 265 (section 9) both azygos veins are reduced, but the 
right trunk (S) has mamtamed itself as the principal vessel, stiU 
connected by the interazygos anastomosis (16) with the very much 
smaller left azygos (6). Ventral to the veins, on each side of the 
aorta (7), are the right and left thoracic ducts (36). The right 
duct, as is mvariably the case in this region, is the larger, and shows 
a pointed dorso-medial extension which passes heLd the aorta 
towards the ventral aspect of the interazygos anastomosis. This 
is a further development of the same conditions seen in the 15.5 
nmi. and 17 mm. embryos, in figs. 254, 255 and 259, and is responsible for the formation of the intermediate dorsal lymphatic element seen in the 16 mm. embryo, (figs. 261 and 262) behind the 
aorta, between the azygos veins and the intercostal arteries. 
(cf. especially left side of fig. 262). 

On the left side of fig. 265, ventral to the left thoracic duct, is 
seen a venous radicle (4) in relation to an extraintimal anlage (5). 
In section 1 1 (fig. 266) this space has enlarged. In the succeeding 
sections 15, 16, and 17 (figs. 267, 268 and 269) the same structure 
appears as a well developed lymphatic channel (61), in the root 
of the dorsal mesentery, and in section 18, (fig. 270) it opens into 
the left thoracic duct. It marks one of the points of connection 
of the mesenteric lymphatic plexus with the thoracic duct, which 
leads to the ultimate dififerentiation of the postazygos segment of 
this channel. The anlage is the same previously noted in the 16 
mm. embryo, (4 and 5, in figs. 261 and 262, series 96), and in the 
15.5. mm. embryo, series 143 {61 in figs. 257 and 258). 



DEVELOPMENT OF THE THORACIC DUCT 149 

Fig. 266 (section 11) is taken at the level of a pair of intercostal 
arteries (j?), which perforate the interazygos anastomotic plexus 
{16) and separate the same from the azygos trunks. The dorsomedial extension of the right thoracic duct towards the interval 
between the interazygos channel (16) and the dorsal circumference 
of the aorta (7) has increased. In section 15 (fig. 267) it has 
crossed to &ie mesal side of the right intercostal arterj'- and occupies part of the area filled in the preceding sections by the interazygos anastomosis. This latter is reduced to insignificant 
remnants. The left azygos vein (6) appears as a minute channel 
between the left intercostal artery (;?) and the left thoracic duct 
{S6). It can be traced in the same condition in the succeeding 
sections. 

In sections 16, 17 and 18, (figs. 268, 269 and 270) the intermediate l3rmphatic channel appears along the dorsal circumference of the aorta, between the intercostal arteries, which now 
pass through meshes separating the three chief channels of the 
lymphatic plexus, viz. the left and right thoracic ducts and the 
intermediate supra-aortic lymphatic. 

The three last figures of this series show very clearly, by comparison with figs. 261 and 262, the advances in lymphatic development, and the recession of the azygos system, especially of the 
left azygos vein, in passing from the 16 mm. (series 96) to the 19 
mm. stage (series 253). The latter presents practically adult 
conditions in both the venous and the lymphatic systems. 

It only remains to be noted that, in the adult cat, the right azygos vein shifts secondarily dorsad to a submuscular prevertebral 
anastomotic venous chain at the 9th or 10th costo-vertebral level, 
and thus affords the opportunity for the greater development of 
the caudal part of the right thoracic duct which replaces the original azygos channel and establishes connection with the abdominal 
lymphatics, forming the above defined ''Post-azygos segment of 
the thoracic duct." 

It is not the purpose of the present paper to enter into the 
development of the abdominal connections of the thoracic ducts. 
This subject requires a minute consideration of the conditions 
encountered in the adult manrntial, and is hence properly reserved 
for future detailed consideration. 



150 DEVELOPMENT OF THE SYSTEMIC LYMPHATIC VESSELS 

Junction of azygos and preazygos segments of the thoracic ditct 

These segments of the main adult lymphatic channel usually 
unite by end-to-end fusion in embryos between 15 mm. and 16 
mm. crownrump measure, although, as previously stated, the 
establishment of a continuous lymphatic channel may be delayed 
in individual instances beyond this period. 

Figs. 271 to 275 inclusive show five successive transverse sections of this junctional area of the two segments in the cephalic 
portion of the dorsal mediastinal region in a 15.5 mm. cat embryo 
(series 143, slide xii, sections 22, 23, 24, 25 and 26, X 200). 

Fig. 271 (section 22) contains the right precava (S) and the left 
azygOvS-C^uvierian arch (ff), with the cephalic termination of the 
interazygos plexus (15,) dorsal to the oesophagus (8). The caudal 
extremity of the preazygos segment of the thoracic duct (36) is 
seen on the loft side, and continues in the next section (fig. 272) as 
the link between the preazygos and azygos segments of the duct 
{35, 36 in fig. 272). In the following section 24 of this slide (fig. 
273) the darker area dorsal to the lymphatic channel marks the 
blind cephalic end of the left azygos arch, and hence characterizes 
the lymphatic channel (36) as the beginning of the azygos portion of the duct. In fig. 274 (section 25) the left azygos arch 
(dorsal 3) is opened by the section and receives the terminal of 
the cephalic end of the interazygos plexus (16) seen in the three 
immediately preceding sections (sections 24, 23, and 22, figs. 
273, 272 and 271). We are therefore now at the cephalic end of the 
azygos segment of the thoracic duct (36), ventral to the azygos 
vein (3) and the interazygos anastomosis, and can trace the same 
unintorniptedly fn)m this point cephalad into continuity with the 
beginning of the preazygos channel (55), as seen in sections 23 and 
22, figs. 272 and 273. 

In the following section (26, fig. 275) the left azygos arch (S) 
is fully opened in its turn ventrad to join the left precaval vein, 
and the azygos segment of the thoracic duct (36) occupies the 
typical position of this period, between the ventro-medial aspect of 
the right azygos trunk (5) and the dorso-lateral circumference of 



DEVELOPMENT OP THE THORACIC DUCT 151 

the oesophagus (S), trending sinistro-cephalad into the Ime of 
the preazygos segment {36, m figs. 271 and 272). 

Reference to the dorsal view of the reconstruction of this embryo (fig. 171) shows that the azygos segment of the thoracic 
duct (36) has united with part of the caudal division of the preazygos chain of lymphatics (35), cephalad of the interazygos anastomosis, into a continuous lymphatic channel, although the con.tinuity with the main preazygos segment has not yet been completely established. In other words this condition has been very 
nearly, but not quite, attained. Some of the preazygos elements 
(36) have already fused with the azygos segment, thus carrying 
the latter cephalad beyond the interazygos anastomosis into the 
territory of the preazygos portion of the thoracic duct. 



PART II, PL.\TES 

FIGl RK8 194 TO 275 



KIOrRKS 194 AXl) 195 

191 Transvorso scM-tion of iiiiddlo thoracic region of 11 nini. cat embryo; 
(series 213. slide XI, section 9) X 225. 
195 Same, section 10. 

1 Syini)athetic nervt*. 

'i Right azypos vein, thoracic portion. 

6 Left azyjjos vein, thoracic portion. 

7 .\orta. 

S Oesojihagiis. 
34 Ventro-medial azygos plexus. 



FI(;URKS llHi AM) 197 

196 Siune, section 27. 

197 Same, section 29. 

1 Sympathetic nerve. 

2 Intercostal arterv. 

3 Right azygos vein, thoracic portion. 
Left azygos vein, thoracic portion. 

.'U Ventro-medial azygos plexus. 



FIGURES 198 AND 199 

198 Transverse section of middle thoracic region of 12 mm. cat embryo, 
(Reries 217, slide XI, section 27( X 225. 

199 Same, section 28. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

34 Ventro-medial azygos plexus. 



FIGUKES 2(K) AND 201 

200 Same, s(Mtion 2). 

201 Samo. slide X. section 18. 

1 Sympathetic nerve. 

2 InterscKniental arteries. 

3 Right azygos vein. thoraci<* portion. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

34 Ventro-nuMlial azygos plexus. 



FIGURES 202 AND 203 

202 Same, section 30. 

203 Same, section 31. 

1 Sympathetic nerve. 

3 Right azvKos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of develop
ing and replacing lymphatic space, 
o Extraintimal or perivenous lymphatic space surrounding degenerating embryonal vein. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

8 Oesophagus. 

34 Ventro-medial azygos plexus. 



FIGURES 204 AND 205 

204 Transverse soction through iniddlo thoni^'ic region of a 13.5 mm. cat 
embryo; (.series 189. slide X. seeti(m 15) X 225. 

205 Same, section 10. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic ])ortion. 

6 Left azygos ve.n, thoracic portion. 

7 Aorta. 

S Oesophagus. 
34 Ventro-medial a/ygos jilexus. 



FKUJKKS 2(Mi AND 2()7 

206 TraiisvcTsc Miction through middle thoracic rogion in a 13.5 mm. cat 
embryo, ' scries 7(). slide XI, section 15) X H(K). 
2()7 Sjune. section Hi. 

3 Right azygos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of develop
ing and replacing lymphatic space. 

5 Kxtraintimal or perivenous lymphatic space surrounding degener
ating embryonal vein 

7 Aorta. 

8 Oesophagus. 

15 Interazygos venous plexus. 



FI(;i KKS 2(IS AND 2()9 

'J{)s Sjiiiir. «»i*rn«u 17. 
NH» S.iiiu-. Motion !*). 

■« hitri'smtiuMiiul artorio>. 

.1 Kmht :uvKi»s \oin. thorarir pi>rli<)n. 

I VtrophviiiK oinbryoual vein, forming kernol in interior of develop
iiiK hihI ivplHi'ing lymphatic vein. 
» KvtraiiiiiiUHl i>r jHTivenous lymphatic space surrounding deKenor
atiii^ cml>rvoiial voin. 
(I Lcl't a/.yi5o> vein, thoracic {xisition. 
/ Voria. 
\ lVMipha\;UN. 

|.'» lhtoniJi>nt»^ venous plexus. 



P^IGURES 210 AND 211 



210 Same, section 21. 

211 Same, section 22. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of develop
ing and replacing lymphatic space, 
o Extraintimal or perivenous lymphatic space surrounding degenerating embryonal vein. 

7 Aorta. 

8 Oesophagus. 

15 Interazygos venous plexus. 



FIGURES 212 AND 213 

212 Same, section 23. 

213 Same, section 28. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

8 Oesophagus. 

15 Interazygos venous plexus. 



FIGURES 214 TO 217 

214 Transverse section through middle thoracic region in a 14 mm. cat 'I 
embryo, (series 214, slide XIV, section 15) X 225. 

215 Same, section 16. 

216 Same, section 17. 

217 Same, section 19. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space sourrounding degenerat
ing embryonal vein. 



FIGURES 218 TO 221 

218 Same, section 20. 

219 Same, section 22. 

220 Same, section 26. 

221 Same, section 27. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 



FIGURES 222 TO 225 

222 Same, section 28. 

223 Same, section 32. 

224 Same, section 34. 

225 Same, section 1. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerat
ing embryonal vein. 

6 Left aeygos vein, thoracic portion. 

7 Aorta. 

8 Oesophagus. 

16 Interazygos venous plexus. 



FIGURES 226 TO 229 

226 Same, section 2. 

227 Same, section 3. 

228 Same, section 4. 

229 Same, section 5. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerating 

embryonal vein. 



FIGURES 230 TO 233 

230 Same, slide XV, section 10. 

231 Same, section 11. 

232 Same, section 14. 

233 Same, section 16. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerating 

embryonal vein. 

6 Left azygos vein, thoracic postion. 

7 Aorta. 

8 Oesophagus. 



FIGURES 234 TO 237 

234 Same, section 19. 

235 Same, section 21. 

236 Same, section 27. 

237 Same, section 28. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerating 

embrvonal vein. 



EXPLANATION OF FIGURES 238, 239 AND 240 

238 Same, section 29. 

239 Same, section 30. 

240 Same, section 31. 

4 Atrophying embryonal vein, forming kernel in interior of developing and 
replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degenerating 
embryonal vein. 



FIGURE 241 

241 Transverse section of lower thoracic region of 14 mm. cat embryo 
(series 127, slide X, section 3) X 225. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

8 Oesophagus. 

34 Ventro-medial azygos plexus. 



FIGURES 242 AND 243 



'il^ 242 Same, section 4. 

243 Same, section 10. 



1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

8 Oesophagus. 



FIGURES 248 TO 251 

« 

248 Same, section 19. 

249 Same, section 20. 

250 Same, section 21. 

251 Same, section 22. 

4 Atrophying embryonal vein, forming kernel in interior of develop
ing and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degen- ^i 

crating embryonal vein. -^ 



» 



FIGURES 252 AND 253 

252 Transverse section though lower thoracic region of a 15.5 mm. cat embryo, 
(series 143, slide XVIII, section 7) X 225. 

253 Same, section 11. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

34 Ventro-medial azygos plexus. 
36 Thoracic duct, azygos segment. 



FIGURES 254 AND 255 



254 Same, section 12. 

255 Same, section 13. 



1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

36 Thoracic duct, azygos segment. 



FIGURES 256 AND 257 

256 Same, section 14. 

257 Same, slide XVII. section 31. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

34 Ventro-medial azygos plexus. 
36 Thoracic duct, azygos segment. 
51 Mosentoric lymphatics. 



FIGURES 258 AND 259 

258 Same, section 32. 

259 Transverse section or lower thoracic region in a 17 mm* cat embryo, 
(series 258, slide XVII I, section 1) X 225. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

36 Thoracic duct, azygos segment. 
51 Mesenteric Ijonphatics. 



FIGURES 260 AND 261 

260 Same, section 9. 

261 Transverse section of lower thoracic region in a 16 mm. cat embryo, 
(series 96, slide XII, section 32) X 200. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

36 Thoracic duct, azygos segment. 



FIGURES 262 AND 263 

262 Same, section 33. 

263 Transverse section of middle thoracic region in a 14 mm. cat embryo, 
(series 211, slide XII, section 2) X 225. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Extraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein. 

6 Left azygos vein, thoracic portion. 

7 Aorta 

8 Oesophagus. 

15 luterazygos venous plexus. 
34 V'entro-medial azygos plexus. 
36 Thoracic duct, azygos segment. 



V 



FIGIRES 2CA AND 2r>.5 

264 Same, sect ion 8. 

265 Transverse section of middle thoracic regjion in a 19 mm. cat embryo, 
(series 253, slide XXIV, section <)) X 225. 

1 Sympathetic nerve. 

3 Right azygos vein, thoracic portion. 

4 Atrophying embryonal vein, forming kernel in interior of developing 

and replacing lymphatic space. 

5 Kxtraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein. 
() Left azygos vein, thoracic porticm. 

7 Aorta. 

8 Oesophagus. 

15 Interazygos venous plexus. 
34 Ventro-medial azygos plexus. 
36 Thoracic duct, azygos segment. 



FIGURES 260 AND 267 

266 Same, section 11. 

267 Same, section 15. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 

5 Extraintimal or perivenous lymphatic space surrounding degen
erating embryonal vein. 

6 Left azygos vein, thoracic portion. 

7 Aorta. 

15 Interazygos venous plexus. 
36 Thoracic duct, azygos segment. 
51 Mesenteric lymphatics. 



FIGURES 268 AND 269 

268 Same, section 16. 

269 Same, section 17. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 
• ('} Left azygos vein, thoracic portion. 

7 Aorta. 
36 Thoracic duct, azygos segment. 
51 Mesenteric lymphatics. 



FIGURES 270 AND 271 

270 Same, section 18. 

271 Transverse section of anterior thoracic region in a 15.5 mm. cat embrj'o 
(series 143, slide XII, section 22), X 200. 

1 Sympathetic nerve. 

2 Intersegmental arteries. 

3 Right azygos vein, thoracic portion. 

6 I^eft azygos vein, thoracic portion. 

7 Aorta. 

8 Oesophagus. 

15 Interazygos venous plexus. 

35 Thoracic duct, preazygos segment. 

36 Thoracic duct, azygos segment. 
51 Mesenteric lymphatics. 



FIGURES 272 AND 273 

272 Same, section 23. 

273 Same, section 24. 

1 Sympathetic nerve. 

3 Right precaval vein. 

6 Left azygos-precaval junction. 

8 Oesophagus. 

9 Trachea. 

15 Interazygos venou.s piexu.s. 

35 Thoracic duct, preazygos .segment. 

36 Thoracic duct, nzygos segment. 



FRIURKS 274 AND 275 

274 Same, section 25. 

275 Same, section 26. 

1 Sympathetic nerve. 

3 Right aygos vein, thoracic portion. 

3 Right precava. 

6 Left azygos-precaval junction. 

8 Oesophagus. 

36 Thoracic duct, azygos segment. 



154 SYSTEMIC LYMPHATIC VESSELS IN DOMESTIC CAT 

It is quite true that it is possible to inject the jugular lymph 
sacs in certain manimalian embryonic stages and thus, by grading the preparations, to obtain pictures which might be interpreted 
in the sense of this theory, provided all questions as to the ontogenetic history of lymphatic organization are designedly left out 
of consideration. There may be a royal road to the solution of the 
vertebrate lymphatic problem, but surely the injection method 
has not found it. It will furnish abundant illustrations of a presumably progressive extension of lymphatic development from 
centre to periphery, but no proof of the actual occurrence of the 
process. The tissues of the developing vascular system in mammalian embryos afford at no period and in no region the slightest 
evidence of such an occurrence. On the other hand, the mammalian embryo does offer conclusive evidence of the development of 
mesenchymal spaces, arising independently of the veins, and lined 
by a lymphatic endothelium which is not derived from a pre-existing haemal endothelium. These spaces form the anlages of the 
future systemic lymphatic channels, and they are continuous with 
intercellular tissue spaces limited by the surrounding indifferent 
mesodermal cells which have not yet assumed endothelial character. This relation of lymphatic anlages, lined by lymphatic endothelium, to the intercellular mesenchymal tissue spaces, while 
clearly determined in mammalian embryos, is moreover strikingly 
and diagrammatically demonstrated in reptilian embryos. 

I have given in the preceding pages my reasons for assigning 
an absolutely negative value to injection experiments in determining lymphatic ontogeny. These preparations yield interesting topographical pictures in the different stages, showing the 
extent of continuous lymphatic organization at different periods, 
but they do not touch the problem of the genetic processes responsible for the establishment of a set of vascular channels capable 
of injection. Much of the general confusion of ideas evident in 
discussions of the question arises, in my opinion, from the failure 
to correctly appreciate the value and significance of the lymphheart remnants of venoiLS origin which in the mammal are interpolated as junctional links between the independently developed 
systemic lymphatic vessels and the permanent functional veins. 



SUMMARY AND CONCLUSIONS 155 

It seems difficult, in spite of carefully chosen expressions, to 
make it clear that in my interpretation of mammalian lymphatic 
ontogeny I am not trying to straddle the question of venous or 
non-venous origin of the lymphatic vessels. What we ordinarily 
describe as 'lymphatic channels' both in the embryo and in the 
adult animal I am forced, by the results of my investigations, to 
regard in anmiotes as vessels developed absolutely independently 
of the hsemal vascular system. The association of these channels, 
in the mammalian embrj^o, with certain embryonal venous lines 
is purely a secondary, mechanical and topographical relationship, 
expressed by the condensed term of * extraintimal' development 
of mammalian systemic lymphatic vessels, and absolutely devoid 
of genetic significance. This is, without reference to other vertebrate classes, proved by the development within restricted areas 
in the mammaUan embryo of systemic lymphatic channels through 
the direct confluence of intercellular mesenchymal clefts, not related topographically or in any other sense to the embryonal veins. 
It is true that in the mammal this independent lymphatic genesis 
is extremely limited, and that the majority of the lymphatic vessels develop in close association with embryonal veins, as products 
of the confluence of perivenous extraintimal spaces. But this is 
merely, as shown by comparison with other anmiote embryos, the 
expression of the peculiar relations obtaining in the mammal between the venous and lymphatic circuits of the vascular system, 
developed independently of each other. 

On the other hand, I am trying to give its full value to a hitherto 
unrecognized component of the finished lymphatico- venous 
organization of the mammal. I am trying to establish the extremely reduced and rudimentary mammalian lymphatico-venous 
heart in the position which its phylogeny entitles it to occupy, as 
the link or bond-piece between vertebrate lymphatic and venous 
channels. I desire to make it as perfectly clear as it is possible to 
do in the English language that this does not mean the acceptance 
of a mixed, partly venous and partly independent genesis of the 
lymphatic system as a whole. It merely calls for the morphological recognition of a distinct and valid structure, interposed, as 
the connecting link, between the definite venous channels and the 



166 SYSTEMIC LYMPHATIC VESSELS IN DOMESTIC CAT 

lymphatic vessels, genetically a derivative from the former, but 
in no sense responsible for the development of the latter. It is 
perhaps possible to illustrate my meanmg by a comparison drawn 
from an entirely foreign field. The pronephric, and the subsequent Wolffian duct, in approaching the cloaca, is met by a responsive outgrowth of the latter and eventually gains its permanent opening into the genito-urinary cavity by union with the 
same. Nobody would hold this cloacal horn responsible for the 
Wolffian duct development by a process of 'outgrowth' of 'budding.' The embryonal veins respond in exactly the same way to 
the approach of the independently developed systemic lymphatics. This response in the typical and prevalent mammal takes 
the form of a rudimentary and foreshortened lymphatico-venous 
heart, and continues to function as such throughout the life of the 
individual, as the jugular lymph sac. There is here certainly a 
distinct genetic principle involved. We, to a certain extent, disregard the cloacal participation in the final establishment of the 
Wolffian duct connection with the genito-urinary sinus, because 
the ontogeny of the duct in itself presents such marked and striking stages. In exactly the same general way I believe that we are 
prone to misinterpret the vertebrate lymphatico-venous junctions, 
unless we recognize lymphatico-venous hearts and their remnants 
in their true morphological significance, as links uniting structures genetically distinct and of different origin. In the matter 
here under discussion this does not mean a double genesis for the lymphatic vessels, part derived from the veins, part by mdependent 
mesenchymal confluence of intercellular spaces. This would be 
no more in accordance with the actual facts than a genetic description ascribing a portion of the Wolffian duct to cloacal ' outgrowth,' while another portion is credited to independent development. I would refrain from laying stress on these facts were 
they based on guess-work, but the entire genetic history of lymphatic and venous organization in all amniote types heretofore 
examined is so strikingly consistent and so uniformly constant 
that my personal conviction of the truth of the above statements 
is very firmly rooted. 



SUMMARY AND CONCLUSIONS 157 

Observations made on vascular structure and growth in the 
transparent tails of living anure amphibia have of late been 
offered in support of the theory of contmuous centrifugal lymphatic development from pre-existing venous endothelium. These 
observations recall vividly the corresponding historical period 
in the developmental analysis of the embryonic blood-vascular 
channels, prior to Thoma's classical researches on this subject. 
Sigmund Mayer nearly thirty years ago employed the tails of 
living anure larvae for the purpose of studying this phase of the 
circulatory system. It seems strange that to-day it should be 
equally, or even more, difficult to induce observers to differentiate 
between development and growth of vascular channels. Development means the genesis of the first embryonic anlages of a vascular 
system. When this has once been established its further extension by growth is an entirely different problem which demands 
equally careful and competent observation and presents many 
phases difficult of mterpretation, involving, among others, the 
entire question of the 'specificity of vascular endothelium.' 
Much futile and controversial discussion could be avoided if 
the growing generation of contributors to this subject will restrain their enthusiasm long enough to bear this vital difference 
in mind. 

On the other hand, the theory which regards the lymphatic 
channels of the mammalian embryo as developing by the coalescence of multiple venous 'outgrowths' or portions of embryonic 
venous plexuses, detached and separated secondarily from the 
parent veins, deserves detailed consideration. 

According to the postulates of this view, the lymphatic endothelium is the direct descendant of the pre-existing hsemal vascular endothelium lining the detached venous elements which enter 
into the formation of the lymphatic channels. The latter, after 
being thus established, make secondary and permanent connections with the venous system. 

It is of course a very easy matter to prove in siiccessive stages 
the topographical correspondence of venous and lymphatic channels, to prove, in other words, that the area occupied by a vein in 
the earlier stages is filled in the following periods by a lymphatic 



158 SYSTEMIC LYMPHATIC VESSELS IN DOMESTIC CAT 

channel. The genetic succession of mammalian lymphatic vessels, developing along and around atrophying antecedent embryonal veins and eventually replacing them absolutely in the topographical sense, has been sufficiently elaborated in the preceding 
pages. There is no question whatever concerning the anatomical 
fact of such replacement. My quarrel lies with the deductions 
which the sponsors of the theory just quoted draw from the evidence of their slides. 

If in an earlier stage they find a vein or venous radicle occupying a definite and clearly circumscribed topographical position in 
relation to surrounding structures, and if they encounter in a later 
stage a lymphatic channel in the identical position of the earlier 
vein, they reason that this topographical coincidence proves 
the direct transformation of the preceding vein into the succeeding lymphatic. They speak of the earlier vein as an 'outgrowth' 
from the main venous channel and describe the same as being ' detached' or 'split off' the latter to form a Veno-lymphatic anlage,' 
which then, by fusion with multiple equivalent detached venous 
elements, forms finally a valid and permanent systemic lymphatic 
channel. It appears to me that in this process of reasoning topography is forced to substitute for histogenesis, and that the vital 
intermediate genetic stages, which finally produce the result under 
discussion, have been disregarded. I believe that this error in 
deduction is based on perfectly correct but insufficient premises 
and is due to the lack of sufficient material capable of demonstrating the intermediate histogenetic stages through which the replacement of a venous by a lymphatic channel is accomplished. There 
are many individual embryos of certain stages, which, interpreted 
by themselves, tend to support strongly the hypothesis of direct 
conversion of venous into lymphatic anlages. It requires a very 
large number of embryos of approximately the same age in order 
to demonstrate the true genetic processes governing the early 
relations of the venous and lymphatic channels in the mammalian 
embryo. Hence the futility of reasoning, from a few human embryos, concerning primate lymphatico-venous relations, which 
we know, from the already ascertained conditions in adult platyrrhine and catarrhine forms, present one of the most complicated 



X '■ '--





SUMMARY AND CONCLUSIONS 169 

and involved problems in the entire genetic history of mammalian 
vascular organization. 

I am convinced that the theory of direct derivation of the mammalian systemic lymphatic vessels from the embryonal veins is 
utterly wrong and that it is based primarily on insufficient observation. It lends itself to an easy interpretation of a relatively small 
number of mammalian embryos of each appropriate stage, but 
fails utterly in reckoning with the conditions presented by a large 
consecutive series of the critical periods. 

I will analyze this view on the basis of the material discussed 
m the preceding pages, first m the region of the thoracic duct approach of the jugular lymph sac and in the preazygos segment 
of the thoracic duct, and subsequently in the azygos district of the 
latter. 

I. THORACIC DUCT APPROACH AND PREAZYGOS SEGMENT OF THfe 

THORACIC DUCTS 

The terminal portion of th^ thoracic duct has been described 
as developed by confluence of venous outgrowths, arising along 
the dorsal surface of the left common jugular and innominate veins 
in the earlier (14 mm.) stages, which occupy the same relative 
position with respect to the main venous channel, the thyrocervical artery and the sympathetic nerve as does the thoracic 
duct in the later (16 mm.) stages. 

In my opinion the so-called ' outgrowths' arising from the main 
venous trunks are the terminals of dorso-medial tributary branches 
entering the same, and have nothing to do with the thoracic 
duct. They are part of the prevertebral capillary plexus in relation in this stage to the dorso-medial surface of the main venous 
channels, as described m detail in the second part of this paper 
dealing with the development of the preazygos segment of the thoracic duct (supra, p. 84). This opinion is based on the fact that in 
many 14 mm. embryos sections through this region show the socalled ' venous outgrowth' and the thoracic duct approach of the 
jugular lymph sac coexisting side by side. 

As previously described in detail (supra, pp. 56 to 77) the thor


160 SYSTEMIC LYMPHATIC VESSELS IN DOMESTIC CAT 

acic duct approach of the jugular lymph sac, in certam typical 14 
mm. embryos, extends as a curved blunt conical process mesocaudad for some distance between the main vein and the thyrocervical artery, towards the interval between the former and the 
sympathetic nerve, where it ends blindly. Mesad of the thoracic 
duct approach the internal and common jugular veins receive a 
number of dorso-medial tributary radicles of the above mentioned 
prevertebral venous plexus. Now, it will depend altogether upon 
the degree of development of any particular embryo, and the selection of the sections, as to whether both the thoracic duct approach 
and the dorso-medial tributary terminal appear side by side in the 
same field, or whether one or the other, or both are absent at the 
particular level examined. Thus in a 14 mm. embryo (series 122, 
slide ix, section 28, fig. 58), the dorso-medial tributary (16) of the 
main vein (left internal jugular, 25) together with the thoracic 
duct approach of the jugular lymph sac {12), are both present in 
the typical relation to the thyro-cervical artery (24) and the sympathetic nerve (1). Traced back in series 122 to section 21 of 
slide ix (fig. 57) the thoracic duct approach (12) is seen to arise 
from the dorso-mesal aspect of the caudal end of that portion of 
the jugular lymph sac, which, as the terminal of the ventral di\'ision 
of the entire structure, forms the jugular approach (IS). 

But since in section 28 of slide ix of series 122, this portion of the 
future thoracic duct (lymph sac segment) is present in the classical 
position between thyro-cervical artery and sympathetic nerve, 
dorsal to the common jugular vein, together with the well developed 
dorso-medial venous tributary {16), it must become evident that 
the latter cannot be regarded as a 'venous outgrowth' representing the anlage of the thoracic duct, since it is manifestly impossible 
to include the ' anlage' of a structure and the actual structure itself side by side in a single section. 

As a matter of fact, a selection of sections in this neighborhood 
in series 122 (14 mm.) will furnish all possible combinations of the 
venous dorso-medial tributary of the internal and common jugular 
vein and of the thoracic duct approach of the jugular sac. 

The two structures, as can be clearly seen, both occupy in sections at the proper level the topographical position along the dor


SUMMARY AND CONCLUSIONS 



161 



sal aspect of the main vein and between the thyro-cervical artery 
and sympathetic nerve, which has been alone employed as the 
basis of the conclusion that, in comparing the 14 mm. and 16 mm. 
embryo, the thoracic duct develops from a portion of the dorsomedial plexus, secondarily split off from the main vein. 

Thus, for example, the series 122 imder discussion, if employed 
for purposes of topographical comparison with a 16 mm. embryo, 
should be represented by the following sections : 



1 
2 

3 
4 
5 
6 



BXRIB8 



122 


IX 


122 


ix 


122 


X 


122 


X 


122 


X 


122 


X 



8LIOK 



sscnoN 



[' 



nouRS 



21 


57 


28 


58 


7 


59 


9 


60 


12 


61 


13 


62 



1. It will be seen that in section 21 of slide ix (fig. 57), the interval between thyro-cervical artery (£4) ^uad sympathetic nerve (i) 
is occupied by the thoracic duct approach (IB) directed meso-caudad from the jugular lymph sac. 

2. In section 28 of the same slide (fig. 58), the thoracic duct 
approach (12) has separated from the sac, and appears, as the free 
terminal of the future adult duct, mesad to the thyro-cervical 
artery (24)- Further dorso-mesad is a venous tributary (16) 
approaching the main vein. Elements of the mesal peri- and interneural venous plexus are also seen. 

3. Section 7 of slide x (fig. 59) shows, in the interval between the 
thyro-cervical artery (24) and the sympathetic nerve (1) the section of the thoracic duct approach (12) close to the dorsal circumference of the common jugular vein (26), 

4. In section 9 of the same slide (x) (fig. 60), the blind end of 
the thoracic duct approach (12) is still seen on the mesal side of 
the thyro-cervical artery (24) f while further mesad the common 
jugular vein (26) receives the terminals of the dorso-medial venous 
plexus. Here, in other words, the Venous outgrowths' or 'anlages of the thoracic duct,' and the thoracic duct approach of the 



162 SYSTEMIC LYMPHATIC VESSELS IN DOMESTIC CAT 

jugular lymph sac appear side by side, dorsal to the left common 
jugular vein, between the thyro-cervical artery and the sympathetic nerve. 

5. Section 12 of the same slide (fig. 61) is caudal to the blind terminal of the thoracic duct approach. A radicle of the dorso-medial venous plexus {16) lies close to the dorsal ^ircimiference of the 
common jugular vein (26) between the thyro-cervical artery (24) 
and the sympathetic nerve (i), approximately in the situation 
occupied in the sections further cephalad by the terminal of the 
thoracic duct approach. 

6. In the following section (fig. 62) this venous tributary opens 
into the main vein. 

A comparison of the structures labelled respectively 16 and 12 
in figs. 61 and 59 will show their close topographical correspondence 
and will suffice to indicate how easily the latter, a valid portion of 
the future thoracic duct, might be confused with the former, a 
dorso-medial venous terminal. Hence, in comparing successive 
stages, the greatest care is necessary in order to avoid the mistake 
of considering a lymphatic channel of the later period to be the 
direct derivative of a ^venous outgrowth' as seen in an earlier embryo. Other embryos of this stage will give equally conclusive 
pictures of the juxtaposition of thoracic duct approach (12) and 
dorso-medial venous tributary (16) in their various mutual relations (figs. 41, 42, 49, 50, 55). 

Of course, caudal to the level at which in this stage the thoracic 
duct approach ends blindly, and before the independent lymphatic 
channels, which are subsequently (15 mm. and 15.5 mm.) to join 
it, are developed, the sections will only show the dorso-medial 
venous branches entering the main channel 

But these venous terminals of a well defined plexus are in no 
sense ' outgrowths' from the veins, nor should they be considered 
as anlages of a lymphatic structure which does not appear in the 
particular section figured, because it has not as yet developed at 
that particular level, although, as in the case in point, it may be 
perfectly evident and coexisting with the 'venous outgrowths' 
few sections further cephalad in the same embrj^o. 

The venous plexuses, both in the prevertebral and in the ventral 



SUMMARY AND CONCLUSIONS 163 

mediastinal region, which form the basis for the extraintimal lymphatic channel development in the correlated segments of the 
thoracic ducts, are sufficiently described above (p. 85). 

There is no question that the mtemal and common jugular veins 
and the innominate vein receive, along their mesal and dorsomesal aspects duringihe 13 and 14 mm. stage, numerous tributaries 
of these two plexuses, as indicated above schematically in fig. 101. 
These terminals cannot, however, be interpreted as ' outgrowths' 
of the main venous line, constituting the venous anlages of the 
thoracic duct in this region and subsequently uniting to form the 
continuous channel of this duct in its preaortic segment. They 
are a direct caudal continuation of the extensive inter- and perineural venous plexus connected, cephalad of the thoracic duct 
level, with the mesal aspect of the internal jugular vein throughout nearly its entire extent. 

The elements of these early venous plexuses serve as lines of 
extraintimal perivenous lymphatic development. 

Both in the prevertebral region cephalad of the aortic arch and 
in the ventral mediastinal area, as above described (pp. 84 to 110) 
the extraintimal anlages of both channels, the preazygos segment 
of the thoracic duct doraally, and the mediastinal trunk ventraUyy 
can be followed in the proper stages from their earliest inception 
to their full completion and union with each other. 

The lymphatic channel system in both areas, as in all other 
regions of the body, is at first very extensive and plexiform, composed of a larger number of intercommunicating spaces. Later 
the definite channel, smaller in cross-cut area and more direct 
in course, crystallizes along definite static lines out of the preexisting lymphatic network, just as we now know that hsemal 
channels do. In other words, the systemic lymphatic channels, 
as would be expected, repeat in their development the ontogenetic 
stages of the haemal channels. Both sets of vessels, lymphatic 
as well as hsemal, result from the condensation of an antecedent 
plexus along definite and determined lines and thus give rise to 
the characteristic vessels of the adult. 

In this entire process there is never a question of the direct 
implication of a vein in the formation of a 'ymphatic space. The 



164 SYSTEMIC LYMPHATIC VESSELS IN DOMESTIC CAT 

majority of the spaces develop, as above described, extraintimally 
along or around a venule, but at the same tune a considerable number of these spaces develop as independent mesenchymal clefts 
not directly related to a degenerating embryonic vein. The embryonic history of this portion of the mammalian lymphatic system, up to the jimction of the completed preazygos segments of 
the thoracic ducts, includmg their ventral mediastinal tributary, 
with the thoracic duct approaches of the left and right jugular 
lymph sacs, is, as above stated, clearly shown in cat embryos of 
between 13 and 15.5 mm. and need not be repeated here. 

Comparison of the 13 and 14 mm. stages with slightly older 
embryos (15 mm.) definitely proves the correctness of the view 
just expressed. In the course of further development the thoracic 
duct approach, turning ventro-mesad into the neuro-venous interval between sympathetic nerve and common jugular vein in 
proceeding latero-mesad across the dorsal aspect of the latter 
vessel, necessarily intersects the line of the dorso-medial venous 
tributaries. Its blind terminal must exchange the position which 
it occupies in the earlier (13-14 mm.) stages, lateral to the dorsal 
somatic venous branch, for one situated on its mesal aspect, if 
the vessels are fimctional venous tributaries and not, as has been 
held, venous anlages of the future thoracic duct in this region. In 
other words, they should continue in the later stages side by side 
with the thoracic duct more fully developed, if they have not become detached from the main vein to form by fusion the lymphatic 
channel. This is seen to be the case, for example, in the sections 
of the 15 mm. cat embryo (series 245) shown in figs. 79, 80, 81 and 
82. The thoracic duct approach (12) here has extended further 
meso-ventrad into the recess between sympathetic nerve (1) and 
common jugular vein (26) and now lies on the mesal aspect of the 
ventro-medial venous tributary (16) which opens into the main 
vein in fig. 82. Fig. 90 shows clearly in the dorsal view of the 
reconstruction of this embryo the lymphatic channel {12-S5) 
intersecting at an acute angle the coexisting dorsomedial tributary 



Sl'MMAUY AND CONCLUSIONS 165 

TI. AZVCIOS SEGMENT OF THORACIC Dl'C 'T 

The genesis of the azygos segment of the thoracic ducts is in 
my estimation the region in which the vahdity of divergent views 
as to systemic lymphatic development can l)est b(* tested. 

Certain mechanical and genetic conditions combine to make 
the investigation of the development of the thoracic ducts in this 
region perhaps difficult in one sense, while in another the results 
of thorough investigation are most conclusive and convincing. 

Part of the difficultv refen*ed to lies hi the relativelv small 
amount of the retro- and peri-aortic space available for the development both of the azygos veins and of the subsequent lymphatic 
ducts replacing the same to a large extent. Again, the process 
of systemic lymphatic development hi this n^gion appears to proceed with great rapidity. The first anlages of the thoracic ducts 
in a given stage are succeeded in stages only slightly older by well 
marked longer segments of the future lymphatic channel. On the 
other hand, the observer lias the advantage^ of dealing with a circumscribed region and with axial venous trunks, which, both in 
their main line and in their tributaries, are remarkably constant, 
regular and easily distinguished. 

As above stated, in the earlier stages a ventral tributary plexus 
of the azygos veins drains the periaortic region. In later stages 
this ventral venous plexus in large part disaj)pears, a bilateral 
lymphatic duct occupying its former plac(\ The two conditions 
cover (^ach other absolutely. 

No one, })()ss(*ssing a knowledge of the embryonic venous development of the cat, can examine a number of injections of the thoracic ducts and azygos veins of the adult animal without IxH'oming 
convinced that in course of development the thoracic duct complex, 
caudal to th(» aortic arch-level, rej)laces a large part of th(^ embryonic azygos venous system, and comes to occupy absolutely its topographical j)osition and relation to surrounding structures. The 
relation of the dorsal intersegmental aortic branch(\^ to the* interaz3"gos venous anastomosis of the (*ml)ryo, compared with the 
intercostal arteries of the adult perforating through the meshes 
of the plexiform lymphatic channel of the thoracic ducts, will alone 
absolutely demcmstrate this mutual topographical corresp(mdeiic(». 



166 SYSTEMIC LYMPHATIC VESSELS IN DOBfESTIC CAT 

The only question at issue is the determination of the genetic 
processes through which the embryonic azygos venous plexus is 
replaced by the lymphatic network of the thoracic ducts in the 
adult. 

Some observers have derived this portion of both ducts directly 
from the ventral aspect of the azygos veins by comparing transections of 14 mm. and 16 mm. embryos, and finding in the former 
ventral tributaries of the main channels, whose place in the latter 
is occupied by the thoracic ducts. They hence conclude that 
the ventral azygos plexus, forming Hhe veno-lymphatic anlages' 
of the thoracic ducts, separates at numerous points from the parent 
vein, and that the resulting detached portions of the originally 
continuous venous plexus, secondarily unite to form the channel 
of the thoracic ducts. The latter structures are therefore, in their 
estimation, direct derivatives of the azygos veins and their tributaries. 

The preceding pages give my reasons for regarding this replacement as having occurred in course of the development of the thoracic ducts by confluence of numerous isolated mesenchymal spaces, 
formed along and around the azygos veins and their ventral tributaries, but genetically independent of the latter and lined by an 
endothelium not derived from the pre-existing haemal endothelium. • 

In the region under discussion these mesenchymal clefts develop, 
owing to local conditions, very largely as extraintimal or perivenous spaces accompanying and surrounding the branches of the 
retrograding ventromedial azygos plexus. The resulting thoracic 
ducts thus come to occupy the place formerly filled by the ventral 
azygos venous network, and later are led into direct ventral 
contact with the main azygos veins, which they in their further 
growth to a large extent secondarily replace. 

In the early (11-12 mm. stage) the azygos veins receive on their 
ventral and ventro-medial aspect the terminals of a venous plexus 
originating in the retro- and peri-aortic mesenchyme. While the 
individual embryos offer many striking pictures at various levels, 
I believe that my purpose of demonstrating the genesis of the 
thoracic ducts in this area will best be accomplished by taking 



SUMMARY AND CONCLUSIONS 167 

sections in successive stages which will present approximately the 
same topographical picture, allowing for the necessary changes 
consequent on increasing development. The area to which I thus 
desire to call detailed attention is the mesenchymal tissue, situated 
on the right side of the thoracic aorta, between this vessel and the 
mesal aspect of the right azygos vein, ventral to one of the right 
dorsal somatic (intercostal) branches of the aorta, and under cover 
of the dorsal surface of the oesophagus. 

These limitations, as is well known, define the position of this 
portion of the main thoracic duct of the adult, and consequently 
the development of this structure, however produced, must run 
its course in this situation. The successive stages, which in my 
opinion definitely and conclusively prove the independent extraintimal anlage of this portion of the right thoracic duct, may be 
grouped as follows, and referred to selected illustrations above described in the body of the text in detail : 

A. Vencyus stage. (Embryos from 10 mm. to 13 mm.). Illustrations in body of text: figs. 194 to 203. 

The sections show an extensive ventral and ventromedial azygos tributary plexus. 

B Stage of replacement of ventral azygos venov^ plexiLS by independently developed perivenous or extraintimal lymphatic anlages 
which accompany and surround the branches of the antecedent 
venous network, and form the first anlages of the azygos segment of 
the thoracic ducts. (Embryos from 13 to 14 mm.) Illustrations 
m body of text: figs. 204 to 213; 247 to 251. 

1. The earliest anlages of the future thoracic ducts are seen in 
certain sections of the thoracic region in embryos between 12 and 
13 mm. crown-rump measure. I have found these early traces 
almost exclusively on the right side, the sinistral position of the 
aorta appearing to delay their development on the left side. They 
make their first appearance as delicate endqtheliaUined extremely 
sparse and widely separated independent mesenchymal clefts, 
at some distance ventral to the main right azygos trunk and near 
the right lateral wall of the aorta. 

At first they are not clearly related to the co-existing ventromedial tributaries of the azygos. But they soon extend to involve 



168 SYSTEMIC LYMPHATIC VESSELS IN DOMESTIC CAT 

these in the characteristic manner above detailed, and continue 
to develop as extraintimal or perivenous lymphatic spaces gradually replacing the shrinking ventral azygos plexus. 

2. In the succeeding stage (13+ mm.) the aorta sinks more 
deeply into the interazygos interval and is spanned on its dorsal 
aspect by the horse shoe of the abimdant supra-aortic cross anastomosis between the azygos trunks of the two sides. The perivenous extraintimal lymphatic spaces surrounding and accompanying the ventral azygos tributaries have increased in size, and a few 
spaces of the same character begin to make their appearance along 
the ventro-lateral aspect of the main azygos veins. 

3. In the 13.5 mm. embryo the extraintimal anlages replacing 
the ventro-medial azygos tributaries have increased in number, 
united with each other to form a series of longer continuous segments, and have, following the lead of the venules which they are 
replacing, approached nearer to the ventral aspect of the main 
azygos veins, and appear more closely interlocked with the ventromedial tributaries of the latter. 

C 14 w^. stage. Illustrations in body of text : figs. 214 to 240. 

The most instructive and conclusive pictures are obtained in 
embryos of approximately this crown-rump measure. 

The sections are clearer and most immistakable in their meaning 
and the individual spaces have become confluent for longer 
stretches, represe^jting longer segments of the thoracic duct channel which is subsequently to be formed by their continued elongation and fusion with each other. This becomes clearly apparent 
in contrasting the ventral view of the reconstruction of series 76 
(13.5 mm.) with that of series 214 (14 mm.) shown in figs. 188 and 
190. 

The diffuse and scattered elements of the parazygos lymphatic 
plexus anlages in the 13.5 mm. stage have, in the 14 mm. embryo, 
become condensed and united into longer segments representing 
the future line of right axial prevertebral lymphatic drainage. It 
is noteworthy, as an important fact, that notwithstanding the 
clear development of unmistakable longer segments of the future 
right thoracic duct, these anlages are still placed at some distance 
ventro-mesal to the right azygos vein and ventral to the intersegmental arteries. 



SUMMABY AND CONCLUSIONS 169 

The 14 mm. embrj^o represents thus in general the full development of the histological picture of secondary replacement of a 
decadent embryonic venous plexus by the secondarily developed 
extraintimal perivenous lymphatic spaces and channels. 

The following conditions have been noted in individual sections: 

a. Ventro-medial tributary of right azygos connected with main 
vein, detached on left side. 

Anlage of right thoracic duct lateral to right ventral azygos 
tributary. 

b. Ventro-medial tributaries of both azygos veins surrounded by 
extraintimal anlages of both ducts. 

c. Ventro-medial tributaries detached and surrounded by extraintimal anlages of thoracic ducts on both sides. 

d. Ventro-medial tributaries in connection with both azygos 
veins and accompanied by ventro-lateral lymphatic anlages on 
both sides. 

e. Azygos veins without ventro-medial branches or their remnants and accompanied on both sides by the thoracic duct anlages 

/. Azygos veins with ventro-medial tributaries without duct 
anlages. 

g. Azygos veins without either ventro-medial tributaries or 
thoracic duct anlages. 

D. Later transitional lymphatic stages. Illustrations in body of 
text: figs. 252 to 258. 

In the 15 and 15.5 mm. embryo three further developmental 
characters appear: 

a. The earlier more redundant and plexiform lymphatic anlages 
condense into a definite channel of relatively smaller caliber. 

6. The central remnants of the atrophied embryonic vein, 
around which the lymphatic anlages developed, have to a large 
extent disappeared, leaving the lymphatic lumen clear. 

c. The individual and originally separate segments of the lymphatic channels have united into segments of greater length, and 
have approached more closely to the ventral surface of the main 
azygos trunks. The definition of a right and left lymphatic trunk 
with supra-aortic cross anastomoses is beginning to appear, al


170 SYSTEMIC LYMPHATIC VESSELS IN DOMESTIC CAT 

though the former is still the larger and better defined. It occupies the original position between aorta and ventromesal surface 
of the right azygos vein, ventral to the intercostal artery, dorsal 
to the oesophagus. 

E. Definite lymphatic stage. From the 16 mm. embryo on. 
Illustrations in body of text : figs. 259 to 262 ; figs. 265 to 270. 

Here all the thoracic duct anlages have united into the continuous and connected plexiform channel of the thoracic ducts, 
ventral to the azygos trunks, dorsal to the aorta. 

The early independent genetic history of the spaces, which I 
have above described as the first anlages of the thoracic duct 
channels in the embryos of the cat, and the fact that in subsequent 
stages they appear consistently and in every possible combination 
as extraintimal or perivenous mesenchymal spaces, following and 
surroimding the branches of the ventral azygos plexus, exclude to 
my mind the possibility of regarding them as derived directly from 
ventral azygos venous plexus, or from socalled ' venous outgrowi^hs' 
of the main azygos trunks, subsequently detached from the parent 
trunks. 

In the foregoing genetic history of part of the thoracic duct 
lymphatic plexus, by fusion of extraintimal and perivenous mesenchymal spaces, accompanying and surrounding certain of the ventral venous tributaries of the right azygos trunk, the following 
points should be noted : 

1. The portion of the entire adult thoracic duct complex here 
considered develops in its earliest stages at some distance ventromesad to the right azygos vein. It only subsequently, by extending proximad along the venule which it replaces, reaches the position in close relation to the ventral surface of the azygos which it 
occupies in the 16 mm. stage. 

2. In the 13.5 and 14 mm. embryos the radicles of the ventromedial tributary plexus are in the process of being surrounded by 
the growing perivenous extraintimal lymphatic spaces which are 
approaching along this line the ventral surface of the azygos, but 
in the 14 mm. stage have not yet acquired this position. The 16 
mm. embr>''o shows the lymphatic anlages in their definite relation 
to the azygos trunk, and the primitive ventral venous tributary 



SUMMARY AND CONCLUSIONS 171 

along which the lymphatic spaces expanded to reach this position, 
has disappeared. The successive stages of this process can be 
followed in such detail and in such conclusive preparations that all 
doubt as to the accuracy of the statements here made seems to me 
to disappear. It is merely a question of suitable material, accurately fixed, sectioned and stained, and sufficiently abundant to 
offer complete corroboration in a number of series of the same age. 
There can then be no question as to the genetic principles involved. 

3. The portion of the thoracic duct, whose genetic history has 
just been outlined, forms only a component of the entire lymphatic complex entering into the formation of the adult duct. Two 
other equivalent components combine with it to produce the adult 
conditions, viz., a corresponding segment on the left side, developed in the same way in association with the ventral tributary 
plexus of the left azygos vein, and an intermediate plexiform lymphatic reticulum which arises as the result of fusion of extraintimal 
lymphatic spaces formed along the ventral aspect of the supraaortic interazygos venous plexus. 

In addition to these three cardinal elements entering into the 
organization of the adult thoracic ducts, these channels, when once 
they have gained their position ventro-mesad to the azygos trunks, 
grow partly by their own expansion, partly by addition of numerous new extraintimal lymphatic spaces which form along the 
azygos veins, expecially on the left side. 

The eventual reduction of the left azygos vein, and of the caudal part of the right trunk, by transferance of the blood current 
to the vertebral chain, accounts for the topographical relations 
of the replacing thoracic duct complex of the adult. 



172 SYSTEMIC LYMPHATIC VESSELS IN DOMESTIC CAT 

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