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On the origin of the abdominal lymphatics in mammals from the vena cava and the renal veins.

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ON THE ORIGIN OF THE ABDOMINAL LYMPHATICS
IN MAMMALS FROM THE VENA CAVA
AND THE RENAL VEINS
FLORENCE R. S A B I N
If’rom Thc Ancctoiiiical Lnbol atory, The Johns N o p k i n s Uriizwszty
It is a pleasure t o have for study Mr. Kampmeit.r’s ablc and valuable
paper on the thoracic duct, as seen in one of my specimens, in the June
number of The Anatomical Record. His direct dorsal view of a wax
reconstruction of the jugular lymphatics brings out one point better
than my profile reconstruction shown to the American Association of
Anatomists in 1910. This point is the crossing of the thoracic duct
t o the right side which I have often, though not always noted. in injections of later stages. Moreover, his paper is a clear and excellent presentation of the theory of the growth of lymphatics by the addition of
tissue spaces.
My own work on the thoracic duct is t o appear in a forthcoming
number of the Ergebnisse fur Anatomie und Entwicklungsgeschichte,
but I should like to present this preliminary note.
Lymphatics in mammals arise in two places, (1) from the anterior
cardinal veins in the neck, ( 2 ) from the inferior vena cava and the
adjacent veins of the Wolffian body or kidney. The budding of the
jugular lymphatics is from the anterior cardinal veins near the duct
of Cuvier but is not strictly limited to the anterior cardinal veins. I n
different forms the budding may extend along some of the adjacent8
vein?, namely the posterior cardinal, the primitive ulnar and the capillaries that eventually make the root of the external jugular vein. The
lymphatics which bud off from the inferior vena cava, which is a part
of the large vein which connects the two Wolffian bodies, and from some
of the veins in the edge of the Wolffian body grow in three directions.
Those that grow ventral to the aorta make the retroperitoneal sac;
those that grow caudalward, lateral t o the aorta, make the iliac. sacs;
and those that grow dorsal t o the aorta make the cisterna chyli and
the lower part of the thoracic duct. There are therefore two pairs
of symmetrical primary sacs in mammals, the jugular and the iliac,
335
336
FLORENCE R. SABIN
and two median sacs, the retroperitoneal and the cisterna chyli. I t
might be said that there are three different sacs in mammals, the jugular
(paired), the iliac (paired) and the retroperitoneal (unpaired) and these
threc sacs are connected with each other by the cisterna chyli and the
thoracic duct. However as I shall define primary lymph sacs as thosc
which bud directly off from the veins, it is necessary t o include the
cisterna chyli with the primary lymph sacs. The primary lymphatic
sacs and the thoracic duct make the primary lymphatic system.
The thoracic duct arises in part as a down growth from the left jugular
lymph sac and in part from a plexus of lymphatics which buds off from
the veins of the Wolffian body. While the thoracic duct is incomplete,
it is excessively hard to inject. The specimen which I loaned to Mr.
Kampmeier is not a perfect injection since i t has extravasations; it is,
however, the first and until the past month the only injection ever mad(.
of a mammalian thoracic duct before i t is complete. It was niadr indirectly through the jugular sac. I filled the sac with ink and then bent
the h a d forward and to my surprise the ink shot into the thoracic duct.
As mill be readily seen a n injection into the jugular sac almost invariably
runs by the path of least resistance or the physiological path into t h r
veins and does not back into the thoracic duct. Perfect injections of
lymphatic capillaries without any extravasations can be made. as for
example Mrs. Clark’s injection of the jugular lymphatic plexus in thc
chick shown on page 263 of the June number of The Anatomical Record
for this year, 1912, but t o obtain perfection i t is necessary t o xwtch
the entire field of injection under the microscope in ordcr to regulatc
the pressure.
Mr. Kampmeier’s figure 1 shows the jugular portion of the thoracsic
duct which arises as sprouts from the jugular sac. These sprouts form
a plexus dorsal t o the esophagus from which ducts grow downward.
The shorter left duct follows the vein t o the root of the heart and I think
subsequently grows t o the left side of the heart and the left lung. A
longer ductJ crosses t o the right side and is the upper thoracic part of
the thoracic duct.
The abdominal portion of the thoracic duct in the pig buds off from
the two sides of the large vein which connects the Wolffian bodies ant1
forms part of the vena cavn and from the large veins in the capsule of
the Wolffian body itself. Dr. and Mrs. E. R. Clark have shown in tho
,June number of The Anatomical Record for 1912 that the lymphatics
for the. posterior lymph hearts of tht. chick bud off from t h r coccygcnl
vein ant1 i t 5 hranchrs, and these lymphatic buds are filled with stagnant
ORIGIN O F ABDOMINAL LYMPHATICS I N MSMMALS
337
blood by a back flow from the parent vein. These lymphatic buds first
make a plexus out of which the lymph heart is formed. I n the chick
thelymphatics while they are still in the bloodfilledstagegrowout t o form
the peripheral capillaries in the skin. Moreover they are closed vessels,
first because the blood in them is held within the contour of the vessel,
and secondly because a little ink injected into one vessel will fill the
entire lymphatic system and empty into the veins without any extravasation.
I n reworking all of the sacs in the pig, I have found that the primary
buds are packed with blood (fig. 7 in 14) and that the blood empties
gradually so that the sacs are subsequently partially filled and finally
empty. The jugular lymphatics bud off from the jugular veins making
the well known jugular sacs. All the rest of the lymphatics in the pig
bud off from the mesonephritic veins. The retropcritoneal sac comes
off from the ventral surface of the mesonephritic vein in themidline of
the embryo. I found out the fact that the abdominal part of the thoracic duct comes from the same vein by direct puncture of the cisterna
chyli in the blood filled stage. I saw the ink enter the mesonephritic
vein. I have three injections of the abdominal sacs or rather plexuscs
made in embryos 23 mm. long. No one of them is perfect and none
shows the cisterna chyli since the ink around the point of injectioii
obscures it. They all show that the beginning thoracic duct, two symmetrical plexuses along the edge of the Wolfian body and the retroprritoneal sac connect. I shall subsequently describe these injections
more in detail when I can also present views of the veins of the region
as well. For the present I want t o describe the blood filled lymphatic
buds as they appear in 23a which Kampmeicr studied, as well as in
another specimen from the same litter and in a human embryo of about
thtl same stage.
I n the series 23a, which measured 23 mm. in its greatest length in
the fresh specimen the blood packed lymphatic buds are to be setn
in sections at the level of the median mesonephritic vein. They arc
in the angle between the vein and the medio-dorsal edge of the Wolffian
body. These buds while still packed with blood form (1) the iliac lymphatics and (2) the cisterna chyli. I n a seriesmeasuring 22 mm., I
have found the earliest blood filled iliac budr arising from the large
veins in the capsule of the Wolffian body, as wc~llas the dorso-lateral
surface of the mesonephritic vein ncar tht. Wolffian body. I n 23a the
iliac plexus of blood pucakcd lymphatics has groun caudalward along
t,hc dorso-medial border of the Wolffian body as far as the hilum of the
338
FLORENCE R . SABIN
permancnt kidney. This plexus of blood filled lymphatic capillaries
is spreading out in the capsule of the kidney and in later stages I have
injected a plexus of lymphatic vessels from the iliac sac intd the hilum
of the permanent kidney around its pelvis. This explains why the
permanent kidney is supplied by iliac lymphatics, while on the other
hand the retroperitoneal sac spreads into the ventral capsule of the
Wolffian bodies as far as the edge of the reproductive glands. Their
lymphatics therefore grow from the retroperitoneal or prae-aortic sac.
The iliac sac is not complete in 23a; the iliac plexus grows down to a
point exactly opposite the bifurcation of the aorta where it swells into
a sac which I first identified as the posterior sac in 1901 in a n embryo
pig 25 mm. long. From this enlarged end grow three main groupsof
lymphatics, (1) a n abundant plexus of vessels surrounding and following
the umbilical arteries, (2) the femoral and (3) the ilio-lumbar vessels
ivhich together drain the leg and abdominal wall.
The cisterna chyli is not present in 23a, but in an embryo 23b from
the same litter as 23a, the blood filled plexus which arises on either side
in common with the iliac plexus has arched across the midline, d o r d
t o the sympathetic ganglia and the aorta. Immediately dorsal to the
aorta a t the level of the anlage of the adrenal bodies the blood filled
lymphatics have enlarged into a cisterna chyli. I n my article in the
Ergebnisse I have shown this important point, that all of the primary
lymphatics bud into non-vascular zones; if the non-vascular areas are
large, the sacs are large, as for example the jugular and the retroperitoneal s&s in the pig; if the non-vascular areas are small, the sacs are
small, as for example the iliac sac and the cisterna chyli in thc pig.
The cisterna chyli develops opposite the adrenal anlage just a t the tip
of the developing azygos veins. Caudal t o this point the segmental
venous plexus drains through the Wolffian body and the transition zone
is a small non-vascular area. Tracing the thoracic duct by the presence
of the blood, the vessels have not yet grown beyond the region of the
adrenal bodies, the blood filled plexus has, however, grown caudalward
dorsal to the aorta t o a point opposite the hilum of the permanent
kidney.
The rest of the thoracic duct forms rapidly, and is probably complete
a t the stage measuring 25 mm. I have completely reconstructed it
a t 27 mm. The lower segment is always characterized by being an
exceedingly abundant plexus which surrounds the aorta as is shown in
Pensa’s figures (111, while the portion from the heart t o the neck is
often a single trunk or at least a few vessels. I n a third specimen meas-
ORIGIN OF ABDOMINAL LYMPHATICS I N MAMMALS
339
uring 23 mm. in which I washed out the blood vessels with Locke’s solution, the abdominal lymphatics are partially filled with blood and the
veins are empty. This shows that the blood packed stage is a short
one. I n this specimen lymphatics from the retroperitoneal sac are
growing around the aorta t o connect with the cisterna chyli. . Subsequently the main connection is around the cerebral surface of the adrenal.
All of the abdominal sacs become connected with each other.
A new embryo in the Mall collection, No. 460, measuring 21 mm.
is of great interest in connection with the abdominal lymphatics. A
careful reconstruction of this specimen with abundant illustrations
will be of value, but for the present I can only give a brief description.
I injected the embryo with India ink through the umbilicaI artery while
the heart was still beating. The vascular injection is almost perfect.
The embryo was then put directly into bichloride-acetic and the fixation is excellent.
I n marked contrast to the embryo pig of about the same length the
Wolffian bodies are disappearing, being pushed caudalward by the
growing permanent kidneys. Thc cerebral pole of the Wolffian bodies,
now far to the side, lies opposite the large median vein which still drains
the Wolffian bodies. This vein is now markedly assymmetrical, owing
to the enlargement of the right side of it, due t o the vena cava. From
the sides of the median vein extends a plexus of veins t o the permanent
kidneys.
From the ventral surface of this vein in the midline is a group of blood
filledlymphatic buds, lying in the root of the mesentery. This area
is very small in the human embryo, in marked contrast with the
large area of the pig, and the human retroperitoneal or prae-aortic sac
is consequently of small size. It is of considerable interest t o note that
thc connective tissue near these lymphatic buds has wider spaces than
along the rest of the border of the vein. They can, however, be distinguished from the lymphatics. Some lymphatics are growing from
the dorsal surface of the median vein, and, pushing between the masses
of cell? of the sympathetic ganglia, have reached the ventral surface
of the aorta.
The iliac lymphatic sacs are of great interest. They are farther advanced than the retroperitoneal sac, because (1) they are larger and
(2) they are only partly filled with blood. They arise not from the veins
of the Wolfian body but from the veins of the permanent kidney. Along
the dorso-medial border of the kidneys between the kidney and the
segmental veins are two long Sacs, the one on the kft being about 1.8
340
FLORENCE R. SABIN
mm. long. The left sac reached the bifurcation of the aorta; the caudal
part of the right sac is less developed, and the place for it is small, on
account of the size of the vena cava. Instead of a sac there are some
blood packed buds along the vena cava itself.
The cerebral ends of the iliac sacs meet in a small plexus of blood
filled vessels dorsal to the aorta opposite the adrenal bodies. This
marlis the position of the future cisterna chyli. The abdominal part
of the thoracic duct can be traced for some distance in the sections.
The trunk for the jugular sac is present but I do not think that the two
parts have met. Another point of great interest in the specimen is that
it shows many areas of widened tissue spaces along the aorta. They
can, however, be distinguished from the lymphatics.
The question a t issue between Mr. Kampmeier and myself is the
method of growth of the thoracic duct between the two anlagen, the
jugular and the renal segments. I admit a t once that I have not seen
the duct grow in the living form, nor have I mastered tho cJifficu1tiw
of injecting i t so as t o demonstrate its gradual growth from two vt‘nous
anlagen. The isolated spaces shox-n in Mr. Kampmeier’s figure 1, I
submitted to most careful study before the meeting in 1910 and discussed them there; they are endothelial lined and I believe them t o be
lymphatics. I believe that adequate injections would show that they
connect with the rest of the system. It was these vessels which made
me consider whether tlic origin of the thoracic duct was not from a series
of vessels from the azygos veins, but this point has now been clcared
up by finding that the cisterna chyli arises as blood filled buds from the
mesonephritic or renal veins. The fact that the injection mass extravasated just above the long apparently isolatedlymphatic on the right side
is not an unsurmountablc difficulty, for it has been noted by a long list
of observers among whom arc Sigmund Mayer (9), Ranvier (12), MacCallum (8), Bartels (1) and myself (13) that it is an especial characteristic of lymphatic capillaries that tiny sprouts in which extravasations
may readily occur often lead to wide bacs or vesscls. I n fact both
Stricker (16) and Sigmund Maycr have seen blood capillaricxs contract
down t o a thread in a living tadpole’s tail, 50 it is known that endot helium
is contractile.
I n regard t o the method of growth of the intermediate division of
the thoracic duct, I know that the peripheral lymphatic capillarirc grow
by budding of their endothelial wall, having seen them in t h r living
tadpole, I know that the lymphatics in the chick bud off from the veins
and grow to the peripheral cnpillarici in skin a\ closcd endothelial vess~lh
ORIGIN OF ABDOMINAL LYMPHATICS
IN MAMMALS
341
having seen them in the Clark’s specimens. I know as nearly as possible without actually sceing thc process in the living form, that the thoracic duct begins in mammals as a down growth from the jugular sac
and as a n up growth from the cisterna chyli which comes from the meEonephritic or renal veins, I therefore do not believe that its further growth
is by a process different from the rest of the lymphatic and blood vascular systems.
The discovery that all the abdominal lymphatics in mammals come
from the veins of the Wolffian body or kidney brings out the significance
and the importance of Silvester’s (15) beautiful injections in South
American monkeys. He showed that in this one form the renal connections are permanent. It also allows us t o consider the question of the
relation of the mammalian lymph sacs t o the lymph hearts and sacs of
the amphibia. Thc anterior lymph hearts of the arhphibia bud off from
the vertebral veins (Knower (7) and Hoyer ( 5 ) ) and as Knower has
shown gets its muscle from the myotomes; the posterior lymph hearts
of amphibia and birds arise from the coccyges1 veins, they lie against
the myotomes and have muscle in their walls. The anterior lymphatics
of birds and mammals arise from the anterior cardinal vein and do not
develop muscle. The abdominal lymphatics of mammals bud off from
the renal w i n s and form three sacs, the retroperitoneal, the iliac and
the cisterna chyli. These sacs are likr the amphibian lymph hearts
in their most fundamcntal point, namely that they bud directly from
the veins, thcy dift’rr from them in position not, lying against the myotomes and in not dcveloping muscle. They arc’ not analogous t o the
amphibian lymph sacs which are secondary structures, transformed
from lymph ducts. The mammalian sacs therefore might be called
primary lymphatic sacs. As a matter of fact the following is the cmhryological classification. Primary lymph sacas : (a) those which develop
muscle in their wall, forming true lymph hearts, for example the anterior
and posterior lymph hearts of amphibia and the posterior lymph hearts
of birds; (b) those which do not develop muscle, but become partially
transformed into lvmph glands, for example the jugular lymph sacs of
birds and mammals arid the mesonephritic (renal) lymph sacs of mammals. I n a word, primary lymph sacs may become lymph hearts or
lymph glands.
342
FLORENCE R. SABIN
LITERATURE C I T E D
(I) BARTELs, P. 1909 Das Lymphgefsisssystem.
Anatomie des Menschen. Fig. 9.
(2)
BAETJER,
W.
1908 Amer. Jour. Anat. vol. 8.
(3) CLARK.
E. L.
(4) CLARK,E. R.
( 5 ) HOYER,
H.
Bardeleben's Handbuch der
1912 Anat. Rec. vol 6, p. 247 and p. 261.
AND
E. L. 1912 Anat. Rec., vol. 6, p. 253.
1908 Bull. de L'Acad. dcs Sciences de Craronc.
(6) I<AMPMEIER,
0. 1912 Anat. Rec., vol. G.
( 7 ) KNOWER,
H. McE.
1908 Anat. Rec., ~ o l 2. .
( 8 ) ~ I A C C A L L UW.
M ,G.
190243 Arch. f . Anat. und Phys., Anat. Abth., and
Bulletin of the Johns Hopkins Hospital, vol. 14.
(9) RIAIER, SIGMUND. 1885 Sitzungsber. der k. Akad. der Wissenshaften Wien,
Abth, 3, Bd. 91 and 92.
(10) RICCLURE,C. F. W. 1912 Anat.'Rec., vol. 6.
(11) PEXSA1908-1909
Lab. di Anat. norm. della Univ. di Roma, T. 14.
(1'2) RAXVIER1897 Arch. d'Anat. Inicroscopique, T. 1.
(13) SABIN,F. R.
(14)
1901 Amer. Jour. Anat., vol. 1.
1909 Amcr. Jour. Anat., vol. 9.
(15) SILVESTER,
C. F.
1912 Amcr. Jour. Anat., vol. 12.
(16) STRICKER1865 Sitzungsbr. der Math.-Naturwissen. Classc d. k. Akad.,
Wien.
BOOKS RECEIVED
THE ESSENTIALS O F MORBID HISTOLOGY, For the use of Students,
Albert S.Grunbaum, with 22 colored plates and 139 other illustrations, 220 pages
including Index, 1912, $2.00. Longmans, Green and Company, London, New York,
Bombay and Calcutta.
MANISCH-DEPRESSIVES GND PERIODISCHES IRRESEIN ALS
ERSCHEINUNGSFORM DER KATATOXIE, Eine Monographie von Dr. Med.
aurycy Urstein, Warschau, 650 pages, U r b m und Schwarzenberg. Berlin, 1912.
Agents for the United States. Rehni:tn Company, 1123 Broadway, Xew York, $7.50.
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