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Remarks on the lymphatics of the reproductive tract of the female rhesus monkey (Macaca mulatta).

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REMARKS ON T H E LYMPHATICS O F T H E REPRODUCTIVE TRACT O F THE FEMALE RHESUS
MONKEY (MSCACA MULATTA)
GEORGE B. WISLOCKI AND EDWARD W. DEMPSEY
Departments of Anatomy and Physiology, Harvard Medical School,
Boston, Massachusetts
NINE TEXT FIGURES AND ONE PLATE (FIVE FIGURES)
Lymphatics of the female reproductive tract have been investigated extensively in man although interest has been
directed mainly to the collecting trunks and regional drainage.
The score or more of papers pertaining to the drainage of the
different parts of the external and internal genitalia in man
are reviewed by Jossifow ('30) and Rouvihre ( '32) and will
not be presented here.
The question of the pattern and origin of the intrinsic
lymphatic plexuses within the various parts of the mammalian
reproductive tract has, on the contrary, received relatively
little attention.
The ovaries. The intrinsic, injected lymphatics of the human
ovary have been illustrated and described in some detail by
Polano ( '03). The injected lymphatics of the cow's ovary are
well shown in three drawings presented by His (1865) ; Buckel
(1874), on the contrary, in rabbits' ovaries, produced extravasation which he confused with lymphatics. Polano ('03)
succeeded in demonstrating distended lymphatics in the
ovaries of two dogs, by tying the collecting trunks near the
hilus. Miss Anderson ('26) has given a complete description,
accompanied by excellent drawings, of the lymphatics in the
sow's ovary utilizing the method of injection and taking into
account the changes accompanying the oestrous cycle.
341
342
G . B. WISLOCKI AND E. W. DEMPSEY
The faZZopiaN tubes. An account, accompanied by figures
of the injected lymphatics of the tubes in man, has been given
by Kroemer ('04). Miss Anderson ( '27) describes in detail
the injected lymphatics of the fallopian tubes of the sow,
referring, as in her study of the ovary, to the changes accompanying the reproductive cycle.
The ztterus. Intrinsic lymphatic plexuses in the human
uterus have been described by Leopold (1874) and Kroemer
( '06) in injected preparations, and by von FranquB ('06)'
who utilized the proliferation of cancer cells as a means of
detecting the lymphatics. I n two gravid human uteri Schick
('06) also demonstrated by means of injection the presence
of lymphatics. I n animals, the uterine lymphatics have been
injected by Leopold (1874) in sheep, pig and rabbit, and by
Mierzejewski (1879) in cow, mare, sow, sheep, dog and
guinea pig. They have also been investigated by means of
silver impregnation by Hoggan and Hoggan (1883), in a
great variety of mammals.
The vagina. The lymphatics of the vagina appear to have
received very little attention. Cateula ('30, '31) has briefly
described the pathways of the collecting trunks in injected
human material. Poirier (1889), from specimens injected with
mercury, gives brief descriptions of two intrinsic lymphatic
plexuses in the human, one in the mucosa, the other in the
musculature. His observations concern, however, mostly the
collecting lymphatics and the illustrations are highly schematized. Bruhns (1898) investigated the lymphatic collecting
trunks in the vagina, in a series of injected human specimens,
but in addition noticed that the lymphatics arise in a fine
meshed intrinsic network lying immediately beneath the
vaginal epithelium.
T h e s e m u l skiit. The only mention that we find of lymphatics
in the sexual skin of monkeys is the report of Aykroyd and
Zuckerman ( '38) that lymphatic trunks extending from the
sex skin to the groin were outlined upon injecting trypan
red intravitally into the sex skin of one male and several
juvenile female rhesus monkeys.
LYMPHATICS O F FEMALE REPRODUCTIVE TRACT
343
These investigations establish principally that lymphatics
are present in abundance in the female reproductive tract.
With the exception of the two modern studies of the ovary
and fallopian tube of the sow carried out by Miss Anderson,
they leave much to be desired in the way of description and
portrayal of the intrinsic lymphatic plexuses. The figures
accompanying the older articles are with rare exception highly
schematized and limited in presentation. As pointed out in
the beginning, they convey considerable information regarding the collecting trunks and the groups of regional lymph
glands, but fail, f o r the most part, we believe, to give any
adequate pictures of the finer character and distribution of
the plexuses.
Miss Anderson’s articles on ovary and tube are complete as
regards both text and illustrations. They have the added
merit that her morphological findings are correlated with exact data on the reproductive cycle.
Our own incursion into this field is based on an opportunity
we have had of injecting the lymphatics of several rhesus
monkeys, the reproductive history of two of which was known.
Although limited to only a few animals and hence somewhat
fragmentary compared to the large series of sow’s ovaries
and tubes available to Miss Anderson, our injections appear
to be sufficiently satisfactory to justify the presentation of
our findings in a series of carefully executed drawings.
Moreover, no observations exist to our knowledge on the
lymphatics of the reproductive tract of subhuman primates,
in spite of the fact that they have become in recent years
one of the main objects of investigation in the field of reproduction. Finally, upon the basis of quite recent advances in
the knowledge of the functional significance of lymphatics
and the formation of lymph, as well as from recent investigations of the physiology of reproduction, opportunity is given
to present certain ideas, which we considered to be of value,
regarding the specific function of the lymphatics supplying the
female reproductive tract.
344
G . B. WISLOCKI AND E. W. DEMPSEY
MATERIAL AND METHODS
Our material consisted of the reproductive tracts of four
female rhesus monkeys (Macaca mulatta). Two of the animals were juveniles which, from their size and the appearance
of the ovaries, must have been close to sexual maturity. The
previous history of these two was not obtained.
The other two animals were fully mature specimens whose
reproductive history was known. For these two macaques we
are indebted to Dr. Carl G. Hartman m7ho generously placed
them at our disposal. The first (monkey 582) had ovulated
regularly and was killed on the twenty-third day of the cycle ;
its ovaries contained a large corpus luteum. The second
(monkey 609) was a few days over 2 months pregnant.
The technique of injecting the lymphatics was as follows.
The animals were anaesthetized with ether. The symphysis
pubis was split in the midline, the abdomen opened and the
reproductive tract entirely exposed. The animal was killed
at this point. The vagina was cut open near the ventral midline, from the vulva to the cervix and the edges reflected to
expose its interior. Injections were performed by the stab
technique by means of a 2 cc. syringe and a 28 gauge needle.
The fluid injected was India ink diluted one-half with distilled water. After injection the reproductive tracts were
widely excised and placed in 10% formalin. Subsequently
parts of the specimens were dissected under a Zeiss binocular
dissecting microscope at magnification ranging from four
to thirty times. Some of the dissected specimens were then
cleared by the Spalteholz method, or sectioned, and stained
with haematoxylin and eosin.
Attempts were made to display the lymphatics of the
ovaries, uterus, vagina and sexual skin. Not all of the injections were equally successful. Any one familiar with the stab
technique for lymphatics will realize that the spread of the
injection fluid from the initial bleb into the surrounding
lymphatic plexuses is variably successful. I n spite of certain
failures, our efforts were rewarded by a number of excellent
LYMPHATICS OF F E M A L E REPRODUCTIVE TRACT
345
injections from which the illustrations accompanying this
paper were prepared.
By the technique of stab injection one runs a certain risk
of injecting veins instead of, or as well as, lymphatics. Consequently the proof that one is dealing with lymphatic channels must be kept in mind. Our criteria for regarding the
vessels, which we are presenting, as lymphatics rest on the
following considerations : the lymphatics form irregular networks and are consequently much more plexiform than the
veins; they also have thinner walls and are more erratic
in their course and irregular in contour and diameter than
the venous channels. When numerous valves are present,
the lymphatics resemble beaded chains. Moreover, the finer
lymphatic plexuses often originate from characteristic blind
terminal sprouts. Finally, it is usually possible to trace the
lymphatics directly into their collecting trunks and thence into
the regional lymph glands. All of these differences combine
to make differentiation from venous injections possible. I n
the areas selected for drawings we regard the injected vessels
as being exclusively lymphatic, with the exception of the
vagina shown in figure 4, in which we are aware from
histological study of the sectioned specimen that ink, besides
filling lymphatics, was present in slight amount mingled with
blood in some of the veins.
Cognizance must also be taken of the possibility of confusing extravasates, which have spread between collagenous
bundles in connective tissue or between bundles of muscle
fibers, for lymphatics. The stab technique of injecting lymphatics invariably produces an extravasate into the tissue
around the site of injection, and a successful preparation
depends upon the spread of the injection from this local
region into the lymphatics in the fields beyond. An appraisal
of whether one is dealing with patterns of extravasation or
with true lymphatics depends upon the discrimination of
the two conditions by applying the criteria for recognizing
lymphatics which were enumerated above. I n the present
346
G. B. WISLOCKI AND E. W. DEMPSEY
study only those areas in the specimens were utilized where extravasations were regarded as being absent or at a minimum.
OESERVATIONS
The results of our study will be presented in reference
to a series of drawings and photographs of our injected
specimens.
The uagim. Figures 1to 4 illustrate the lymphatic plexuses
of the vagina. Figure 1shows the entire wall of the vestibule
and vagina of a juvenile macaque with the lymphatics injected. The ink gained entry to the lymphatics from two
points of injection: first, from the large bleb of ink in the
tunica propria of the vestibule (lower right hand corner of
figure) and second, from a point of injection near the cervix
(upper left of figure). It will be seen how from these sites of
injection the ink spreads extensively in the lymphatic plexuses
of the mucosa of the vagina and vestibule. The lymphatics of
the vestibule are somewhat larger and coarser than the
delicate, fine-meshed plexus of the vagina proper ; moreover,
they lie apparently in a looser type of connective tissue than
those in the vaginal mucosa and are consequently more difficult to inject without producing extensive extravasation.
Figures 2 and 3 are drawings at higher magnification of
two fields indicated by a rectangle and square in figure 1.
It is seen in figure 2 that the lymphatics form a rich, delicate
plexus situated in the tunica propria. Numerous short,
slightly bulbous terminal lymphatic sprouts appear to connect with the main plexus. I n figure 3 the lymphatics of the
vaginal part of the cervix uteri are shown. They constitute
a delicate plexus similar to the one in the vagina proper. A
photograph of a thick histological section of the wall of the
vagina is presented in figure 14, showing the character of
the injected lymphatics.
Figure 4 illustrates an injection of the lymphatics of the
vaginal wall in an adult macaque on the twenty-third day of
the menstrual cycle. The field is taken from the posterior
vaginal wall where the surface is thrown up into clumps of
LYMPHATICS O F FEMALE BEPBODUCTIVE TRACT
347
conical epithelial papillae. Thc epithelium clothes groups
of connective tissue projections or papillae wliich extend out
from the tunica propria. I n tlie figure the injected lymphatic
plexus in tlicse papillae and the tunica propria of tlie vagina
can be seen. The lymphatics constitute a rich network, extending from beneath the surf ace epithelium, throughout the
Fig. 1 Vagina and wstibulc of a juvenilc rlicsns monkey with the lyiiiphaties
filled hy injection of India ink. x 24.
tunica pi*oipi*iainto the musculan*aiicl outer filnrons coat of the
\Tagilia where collccting trunks ai'e foi.meil. The lymphatics
of tlie vagina of tlic sexually mature animal (fig. 4) are
c~-iclciitlgmucli larger, although appaiwitly no marc abundant,
iiumci.ically, than the vaginal lgnipliatics of the juvenile
macaque (figs. 2 aiicl 3 ) .
T7io z / t ~ r ~ r Tlie
s . patteim of the injected lymphatics of the
uterus of a very tiearly inature, juvenile macaque is showti
in fignw 5. Lgmphatic*s am abutidant throughout the u t e ~ i n e
wall. The enclometrinm contains lymph cliariiiels which form
caliaractcbi.istic ai-cades occii1,yiiig the clcqner three-qnartcw
of the miicosa. Tlic most snpcrficial la:-ei* of miicosa houtiditig
tlie inteiiiitl lumen appeam, on the coiiti-arp, to be devoid of
lympliatics. At the juiictioii of tlic endomcti~iumand muscularis
LYMPTIATICS O F FEMALF. I;EPROI>UCTIT'E TKACT
349
(sti~itnrnsuhmucosum) there is a deiise plexus of lymph
vessels.
The myometrium is richly snpplied n-itli lympliatics which
pass outward constituting an irregular plexus between tlie
interlacing muscle huntlles of the thick vascular laycr of the
muscnlwi*is. A photograph of tliese l~-mpliaticslying bc~twecii
Fig. 3 The lymphatics of tlic vaginal pnrtioii of tlic ccrvix sho\rn iii iiiorc
detail (area of square in fig. 1). >( 3 7 .
the interweaving muscle bundles, and aceompanring the
aclventitia of tlie coiled uterine arteries, is presented in figure
10.
In the place selected f o r di.aming, 17mpliatics have not
been injected in eitlicr the outer muscular layer or in the
scrous membrane. Ncvertlicless exaniination of other parts
350
G. €3. W I S L O C R I A N D E. W. DEMPSEY
of tlie uterus reveals that these layers also contain lympli
channels. The outer ( supravascular) muscle layer possesses
a n intriiisic lymphatic network which anastomoses with that
of the middle (vascular) muscle layer. A t the boundary of
Fig. 4 Tiijrctetl lyiii1)li:itic$ i n t h e \agiiinl nall of an adult rhesus monkey
killed on the titciitF-thiid d:13 of llic eyc.1~. X 10.
tlie middle and ontci. muscular layers, laterally in tlie neighborhood of the broad ligaments, these networks unite to form
collecting truiilis. The begiiiiiiiig of one sucli collectiiig vessel
is seen on the right in fignre 5.
LYMPHATICS O F FEMALE REPRODUCTIVE TRACT
351
A distinct and separate connective tissue layer of the serosa
(subserous layer) is lacking over the entire fundus of the
utcrns of the macaque, the serosal cells resting essentially,
as in man, directly o n the outer muscular layer. Consequently
in this region there is n o special plexus of subserous lymphatics separate from the intrinsic plexus of the musculature.
Around the ceyvis, however, as well a s in the paramctrinm
and broad ligaments, a true siibscrous layer of coniiective
Fig. 3 The lyaipliatic plcruses in the wall of thc uterus of a nearly adult
diesus monkey. The endotnetrial surface is on the left, tlie swosal covering on
the right of tlie figure. Notice the rich plexus of Iyinpliatics at the jiiiiction
of the eiidoinetriuni and tlic muscularis. x 20.
tissue is present in which a separate, delicate plexus of
l:*mphatics can be injected.
TIP gravid iiterzis. The injection of the lymphatics of a
gravid macaque wliich was a few days over 2 montlis pregnant turned out very successfully. The results of this injcetioii arc shown in figures 6, 7 and 8.
The appearance shown in figure 6 was obtained by dissecting away, over a portion of tlie body of the uteriis, the serosa,
besides the most superficial inuscle bundles and the accom-
~pa1i;viiiglynipliatics. The uterus was uiiopciicd so that the
cli.awiiig shows tile lymphatics in tlie middle muscle layer
~vlieiilooltctl at from the outside uiiclci. it binocnlai* disswtiiig
micimcope. Sti4king is the wealth am1 size of the lymph at'1cs.
011 the riglit of the figuiq near tlie broad ligament, tlie lymph
c~liaiincls a i seen
~
joiiiiiig a large collecting truiik, one of
scvcral in tile neighborhood. Tliesc collecting trunks find
thcii. way iiito tlic broad ligamerit arid parametrium.
Fig. 6 The lymphatics of tlic ~nuseulniisof the prcgnant uteius of a rliesus
iiioirkey, seen fioiii the surfaec, a f t e r stripping a n n p the scrosa an(l tlie outer
muscle fibcis. On tlie riglit a tTpic a1 rollcctmg lyiiipliatic is s h o n n passing
t o \ \ a i d tlie bro:itl lignniciit. X 33.
After esaminiiig the lymphatics of the inuscnlature in the
manner described, the uteriis was split open, so that the
successive layers of the uterine wall and placenta could be
observed. Figure 7 represents a cross section through tlie
uterine T I Y ~at
I the site of tlic placenta. T t reveals the lynipliatic plexuses in the muscularis and decidua. It is observed
that the lympliatics a r e abundant in the deeper lialf of the
LYMIPTIATICS O F FE&\TALE 1:EPI;ODUCTIVE
TIC4 CT
353
cleciclna, the so-cdlecl pars spongiosa, Tr-liereas the p r t i o i i
of the tlecidna, dcsigiiatcd as the pars compacta, to Tvliiclr the
fetal l h c e i i t a attaclics, appears t o be devoid of lymphatics.
The 13-mpliatics of the spoiigiosa a r e verv large aiid iiiixnerous
aiicl tend to congregatc in tlie loose ad\Teiititial slientlis of
the coiled ciidometi*ialarteries.
Figure 8 is of a dissection obtained hy separating or
stripping off the muscularis from the clecidua in the region
of the placental site. With tlie muscle removed, one is looking, in the drawing, at the mateixal surface of the decidna.
In this region of separation of muscularis and decidna one
observes a ~vealtl.1of larye lymphatic channels forming a
cleiisc, intricate plexus. Lpmphatics map be seen in the figure
weaving around several tliicli-walled maternal arteries which
supply the placenta.
354
G. 6. U'ISLOCKI
A N D E. W. DEMPSEY
It ~ i l be
l observed, by comparison of figures 6 and 8 with
figure 7, that tlie lymphatics form flattened bands, very broad
arid tortuous when seen in surface view, but resembling narrow clefts when vicwed in cross section. Figure 11 is a
photograph of a histological section through the uterine wall
at the placental site. The rich plexus in the basal portion
of the decidua, at its juiiction with the muscularis, is readily
F i g . 8 A vicvc. of thc rich l p i p h a t i c plexus in tlir decidua, seen after disseetiiig away tlie eiitirc niuscu1:ri is. The lpipliatics are abundant in tlie region
of the spiral arteries wliicli 1)enctrate the decidun. Sevrral cut trunks of tliese
arteyies are sliowii iii the fignie. x 5:.
visible. The injected lymphatics a r e quite sharply demarcated
from another set of clcfts consisting of the flattened and
attenuated uterine glarids wliicli ai*cuninjeeted.
By comparison with the lion-gravid uterus, tlie lymphatic
chaiinels of the gestational uterus, although probably not
numerical1;v increased, a1.e obvious1;v tremendously eiilargcd
in caliber.
LYMPHATICS O F FEMALE REPlXODUCTIT’E TRACT
355
Th e ovaries amd tubes. W e did not undertake iiijectioiis
of the fallopian tubes since they a r e relatively small in the
macaque monkey. The lymphatics were injected, however,
in two pairs of ovaries. We a r e not presenting any figures
of the ovarian lymphatics, because our limited material does
not add essentially to tlie complete study of Anderson on the
sow’s ovary. I n regard to the ovary of a macaque monkey
from the twenty-third day of the cycle contaiiiiiig a large
corpus luteum, the following notations were made. The ovary
is richly supplied with lymphatics. Delicate lymphatics located
in tlie tlieca interna surround the small resting, graafiaii follicles which a r e present at this stage. In the well-developed
corpus luteurn, which is perhaps a week to 10 days old, ribbonlike 1Fmphatics a r e abundantly present in the strands of
theca iiiterna which partially subdivide the luteal mass. A
plexus of lyniphatics is also present in the theca exteriia
which surrounds the corpus luteum. When the intact ovary
was examined under the dissecting microscope, a tiny cap of
aiiastomosing lymphatic vessels was seen on the protruding
pole of tlie corpus luteum, whereas the surface of tlic ovarF
everywhere else was totally devoid of lymphatics. Examiiiatioii of the interior of the cut ovary bears out the coiielusion that the lymphatics, excepting in tlie vicinity of the
former point of rupture of the follicle, do not reach the
snrface of the ovary. The lymphatics associated with both
corpus luteum and follicles drain away from tlie surface into
the interior of the ovary where they anastomose to form
collecting trunks leaving by tlie hilus.
The semial skin. The sexual skin was examined with sonic
interest, because the intrinsic lymphatics of this peculiar
tissue of certain catarrliine monkeys and apes have never been
demonstrated before. Tt was found that from a bleb of ink
introduced into the corium of the sex skin collecting lymphatic
trunks conlcl be readily filled. These led invariably, in the
subcutaneous tissue of the thigh and groin, to sets of inguinal
glands. The intrinsic plexus of the corium of the scx skin
proved, on the contrary, difficult to inject. Nevertheless,
396
G. B. WISLOCICI A N D F,. W. DEMPSEY
repeated trials yielded evciitnal success. In figlire 9 we preseiit
it cleared p r e p r a t i o n of a piece of the sex skin with the lympllatics iiizjected. This specimen is from our pregnant macaque.
The lympliatics constitnte a very dense network of relatively
Fig. 9 111,lecteil IyinpIiatic plcxris i n tlic corium of tlie sexual skin of a
piegnaiit rliesus monkey. P'ioni tlie fiire-iiieshed surface i i e t ~ v o r l cthe 1) niphatics
pass into a coarser lymphatic 1)lexus situatcil beiirntli in the suhrutnneous tissue.
The Eperiiiien i c q p r q i u ~ e dby Rpaltcliolz 's elenring method. x 14.
small calibered lympliatics situated in the corium from which
the lymph is drained into larger channels which r u n in the
subjacent subcutaiieous tissnc. Figure 13 is a photograph
of a histological section through the sex skin, sho~vingthe
iiijected lymphatic plexus.
LT3IPHXTICS O F FEAIILE E E P K O D C C T I Y E TILI1CT
357
DIRCUH8ION
F’mm the f i g u ~ ~its will bc obsci-ved how extensive the
Iyvmpliatic plexnses of the female reproductive tract are.
Their relative abundance compai*cs favorably, if it does not
creii exceed, that of other tissues wliicli are known to be relatively rich in lyvmphatics, f o examl)le,
~
parts of the h:;lstrointestinal and respiratoi-jT tracts, especinlly the iiasophal*;vnx,
tlie corium of the skill, arid the diaphragm.
The question presents itself as to ~ h tlic
y female reproductire tract should he so richly snpplied with lymph at’1cs.
A thought close at halid is that it ma? be coniiected in some
way with the fact that the reprodnctive t ract ~iiidergoes
cyclical changes. The studies G f Aiidei.son o n the sow'^ ovai*ies
and tiibcs clemonstratc, conclusivel;v, that the lymphatics
niideiyo cliaiiges clui*iiigtlic cy.c.1~.IIei- obserrations iiidicatc
calc>arl!- that tlie lympliwtics of the tube undergo cyclical enlargement in caliher, altliongh prohahly riot in actual iinmber.
Injection of the sow’s mesosalpiiis, ampnlla and isthmus xms
m o w complcte and more readily accomplished diu5ng oestrus
and tlie first few clays thereafter. The vessels of the amp~illn
were foiiiid, f o r example, to be twice a s large aiid more
readilp injectahlc clnring opstrus than in the clioestrous int e n d . lloreover, our observations on the gravid macaque’s
uterns indicate that during pregnancy the lymphatics of the
uterine wall undergo tremeiidous hypertrophy, a fact also
noted by Schick ( ’06) in the human.
The above remarks talieii together with certain other recciit
ohservations on tlic pliysiology of the female reproductive
tract offer, we believe, a clue, hitherto overlooked, to explain
the fanctiorial significance of the lymphatics of the f emalc
reproductive tract. It should be iwalled that evidence lias
accumulated iii recent years that around the time of oestlns
the ovaries, fallopian tubes, uterus, vaginal wall, and sexual
skin undergo, t o variable degrees, periodic hypertrophy aiid
swelling. In many parts of the reprocluctive tract this expresses itself as liistologically demonstrable oedema, e g . ,
the oedema of the clccidua at tlie site of implantation (Wis-
358
G . B. WISLOCKI A N D E. W. DEMPSEY
locki arid Rtreeter, '38), tlie oedematous swelling of the sexiial
skin i n the pigtailed macaque and baboon (Krohn and
Zuckerman, '37 ; Aykroyd and Zuckerman, '38), as well as
the changes in water content of the uterus of the rat, indicated
by the stndy of Astmood ( '39). Furthermore, Krohn and
Zuckerman ( '37), Thorn and Harrop ( '37) and others have
recently sliowii that oestrogenic substances have water- and
salt-retaining properties. lloreover, it has been demonstrated
expei~imentallpthat after injection of the sex hormones, certain of the female reproductive tissues become markedly
hydrated ( Aylrroyd and Zuckerman, Astwood) .
This circumstance, we believe, explains the results of Anderson 011 tlir cyclical changes in the caliber of the lympliatics
in the uterine tubes and it accouiits f o r the enormous size of
the lymphatics of the pregnant uterus. I n tissues xliicli par
excellence undergo periodic pliysiological hydration and exliihit histological smelling and oedema, the lymphatics a r e
presumably of the utmost importance. JTTere they not
abundant and capable of undergoing hypertrophy, the oedema
fluid, it might be anticipated, would accumulate and lead
t o patliological changes. Drinltcr and liis associates ('33, '38)
have adduced considerable evideiice to shorn that tlie composition of lymph is that of dilute blood plasma and that
such blood proteins as leave the capillaries to enter the tissue
fluid are removed by tlie Iympliatics. Accepting Drinker's
concept of the protein content of tissue fluid and lymph, one
has to accept, in view of the colloid osmotic pressure of the
blood plasma, that the lymphatics provide the principal means
for the ultimate escape of the 1?i.otcin-containing interstitial
fluid from the tissues. Moreover, Aykroyd and Zuckerniaii
( '38) have reported a high protein content of the interstitial
fluid in the active sexual skin of the female rhesus monkey.
In view of these various considerations we advance the
interpretation that the ahundant lymphatic plexuses of the
fernale reproductive tract and their demonstrated hypertrophy aitd dilatation sabserve the role of reducing the
L Y M P H A T I C S O F FEMALE REPRODUCTIVE TRACT
359
physiological oedema o r hydmtion to which these tissues a r e
subject, allowing them to return to the resting condition.
Other functions which they may exercise a r e probably quite
subsidiary. Miss Anderson, for example, ascribes to the lymphatics of the ovary especially of the corpus luteum, the
role of draining the lutein secretory products. Polaiio ('03)
suggests that the ovarian lymphatics act as an elastic cushion,
or shock absorber, which prevents injury to the gi*owiiig
graafian follicles, wl~ile,just after rupture of a follicle, they
prevent the wall from collapsing completely. Polano cites
no real evidence to support his concept. Regarding the lymphatics of the tube, Anderson suggests that they may absorb
the folliculsr fluid liberated at ovulation which i n the sow
may amount to 1.5 cc. Hartman ( ' 3 2 ) remarks that the tubal
lympliatics a r e of special interest i n coiinection with the fluid
of the bursa and the tubal lumen, since they offer largc
surfaces f o r resorption. We regard it as worth mentioning,
also, that the uterine lymphatics may participate i n the resoiytion of the fluid which distends the uterine lumen a t
ocstrus in the rat and mouse. Grosser ('19) suggests that
the blood vessels a r e arranged to produce some sort of
turgidity of the fallopian tube during ovulation and that the
alternate filling and emptying of the associated lymph spaces
might act as a sucking mechanism. As A4iidersoii points out,
this tlicory may be discarded when the drainage of the tubal
lymphatics is considered. The possible role of the tubal
lymphatics in absorbing foreign material from the lumeii,
mentioned by Anderson, seems to be of doubtful consequeiice
under normal conditions. Similarly the involvement of the
1Tmphatics of the reproductive tract in various inflammatory
diseases can be of pathological importance only. However,
in tissues which become so readily hydrated, the thought lies
closc at hand, that in pathological states, with possible occliision of p a r t of the lympliatics, fibrosis might be an aftermath.
RI.JIJZ {RT
Tlic lyniphatics of the reproductive tract of the female
rliesiis monltcy were injected. Rich intrinsic lymphatic
plcsnscs ai’e demoiistralole in the literus, vagina and sexual
skin. I n tlic lion-gi~avicluterus, conspicuous lymphatic net~vorksare visible in botli the eiiclomctrium and musculai.is. In
pregiiancy these plexuses hypertiwpliy ; the Iympliatics of the
eiidometrinm, although larqe and abundant, arc limited to the
p i x spongiosa ; the compacta and junctional layers of the
clwidua, 011 the contrary, are clcvoid of lympliatics excepting
a few which extend out a short distance in tlie advexltitiixl
shcatlis of the artcrics entering the compacta. The ragina
p s s c s s w ;ivery c h s e iict of lymphatics in its tunica propria.
Similarly the sex-ual skin has a11 extensive network of lymphatics in the corium whicli coiinccts with a coarser nieslieci
plesus lying i n the wbcntaneous tissue.
Reasons a r c adraiicetl f o r loelic~viiigthat tlie rich lymphatic
supply of tlie mammnlinii fcmale reproductive tract is related
nininly- to tlie hydration, or physiological oedema, t o which
ICS are subjcctecl pcrioclicallp under the influence
of the sex liormoncs, more especially, estriii. Evideiice indicates that the lymphatics are hypertrophied during the active
phases of the cycle. The lymphatics serve t o dehydrate the
tissues lo;- removing the l)roteiii-coiitaiiiiiig. tissue fluid and
lieiicc proiriotiiig retn1.n to the resting or dioestrous condition.
1,IrI’El?ATURE C I T E D
I). H. 1926 Lyit1lilintir.s a n d 1llOod T-t.hsel5 of t11r o \ a r y of the SO\\.
Cuincgie (”ontiib. E i n b r ~ o l . ,101. li, pi). 107-1‘74.
-___
192‘7 L>mphntics of the tallopiaii tulic of th c tow. Cariicgie
Coiitiili. Enibr)ol., x o l . 19, pp. 135-148.
1939 (‘li:uiges i n tlir neight a n d water coiitciit of tlir u t e i m
L ~ s r l r ~ ~ oIC.
o D1:.
,
of tlir iioriiinl adult rat. Am. .T. I’h>siol., vol. 186,pp. 162-170.
-kYKROYD, 0. I:., A N D R. Z I r ( ’ l \ F R l I A S 1!138
Fartors iu rcuual-skill otdenin. J.
Plivsiol., rol. 94, pp. 13-25.
f i R U “Ns,
C. 1898 C e h e r (lie L: i ~ ~ l r h g c ~ f ~ dcr
i s s c neihliclini Griiitdlieii iic~lis:
r i ~ ~ i g e~r171erliu11gen
n
ulJcr ( 7 i ~Topogrt~plricder L e i s t e n d r ~ ~ s e nA. I (11.
f . a4i1at. 11. Physiol., i l n a t . AM., lip. ST-80.
L\Nl)rRSON,
L Y M P H A T I C S O F FEMALE I t E P R O D U C T I \ ~ E TRACT
361
1874 TJeluer die Lyniphwege des Ovnriums. Site. Ucr. d. Wiener
Aknd. d. Wiss., vol. ‘TO, Iili. 156-161.
CarrEuL,a, T. 1930 Note sur les Iyiiiiiliatics du vagin. C. R. Soc. anat. dc
P:i,is. Ann. d ’anat. path. e t d’aiiat. iiorni. ni6d-chir., vol. 7,131). 3Tl-572.
____
1930 Nouvelle note siir 1es lyrnphatiques du v a g h C. R. Hoe. allat.
de Paris. Ann. d’anat.-p:itli. c t d’nnat. noriri. in&d.-cliir., 1701. 7, 111).
903-904.
_____ 1931 Les lyniphnticlucs d u ragin. C. R. Roc,. Anat. de Paris. Ann.
d’aiiat.-patli. et d’annt. n o m i . n i b d . chir., ~ o l 8,
. pp. 1187-1140.
DBISKER, (1. I(. 1988 Tlir functioual significance of the 1yniplr:~tic systt.111.
Bull. N ~ \ Yolk
v
h c a d . Med., ~ 0 1 14,
.
1)1>.231-251.
Lglll~ihnlld ~’iSSlleb’lllid.
IIRINIiER, (:. K., A N D hf. E. FIEI,I> 1g,‘{:< I~~niph:XticS,
The Williams and W’illrins Co., Baltiniore.
F R A N QVO~N,
I : ~ 0. 1906 Zur Keniitiiis der Lynipligef~sweder Uterussc~lilriiiillnut
iind tles Tuliencnrriiionis. Verh. (1. deutsch. (;csrllscli. f . Gyli., pp. 438447.
GROSSER, 0. I919 Ovulation uiid In1l)lantation iind die Funktion dcr l’nhe
beiin Xlenschrn. 1Zreh. f . Gyn., vol. 110, 111). 297-32:.
1~.4RTAIAN, c. G. 1933 OvuhtiOn :Illd the transllort a l l t l I7i:ih:lity o f Ov:l x13d
sperin in the female genitsl tract. Cti:iyt. XIV in Sex awl Interiinl
Recwtioiis. Pp. G4T-715. Edited 1)g I.klgur Allell. Tho Willinnis nnil
Wilkiiin Co., Ualtiimore.
HIS, W. 1865 Reobachtiingen i i h r den Rau iles S~~iige:liiere-Eierstocltes. Arch.
f . micro. Anat., vol. 1, ~ q )151-202.
.
HOGGAN,
G., AND F. E. HOGGAS 1882 011 tlic, coiiiparative aiiatoniy of tlic
lynip1iatic.s of tlic utcriis. a. Aiint. a n d Physiol., vol. 16, pp. 50-89.
JOSSIYOTV,
G. iLI. 1930 1)as ~,!.inph~”f~sssysteiii
ilos Nrnsclirii. Gustav Fisclicr,
Jena.
I<ROERLEE, P. 1904 I)ie Lyiii~iliorgaiic~
tlw \vribliclien Genitnlien und ilirc T7ci~iintlerung bei nialigiieii Erkr?iikungen tlrs Utc’rus. Arcli. f . Gyn.,
rol. 7 3 , pp. 57-158.
KROHS,1’. L., A N D 8. ZI:CKEl<MAiY 1937 W a t e r metaholisin in relation to tlir
nicnstriial cycle. J. Phgriol., wl. 88, I ) ] ) . 369-387.
LEOPOLI),
G. 1874 Die Lympligeftisse cics iioriii:llrii iiichtscIi~\-aii~ereii
Utcriis.
Arch. f . Gyn., vol. 6, pp. 1-54.
I~IEEZEJIWSKI,
V. I 879 Rcclicrchcs stir lcs l y i n ~ ~ h : c t i c ~de
~ i eIn
~ couclie so:^
s6reii.e de l’ut6rus. J. d e I’niiat. et de In pliysiol., vol. 13, p11. 201-224.
PCIRIFR,
1’. 1889-18!30 Lynipliatiques drs orgnncs gcnitaux de la femme. Le
ProgrEs medical., vol. 10, (Vagina) pp. 49--493, (Vtvrus) 7 1 ~ 1 . 50!)511, (Cervix) p p . 527 -529> (Ytcrus) pp. 568-569; vol. 11, (Vteriis)
1)p. 41-42, (Ovaries) pp. 6.5-68.
P O 1 8 A N 0 , 0. 1!I03 Ih3itr:igr 2111‘ ~\ll:ltomie der L y i n p h ~ ~ a l i n e n
in1 mciiscll~ic~licn
EitrFtoek. R1oii:itschr. f . Grhiirtsh. ti. Gyixiek., vnl. 17, pp. 281-295,
pi). 466-496.
ROKIVIERE,
H . 1932 Aiint~omiedcs Lyniplintiqiics de 1’Honinic. hl:isson r t Cic,
Paris.
sCHl(”I<, B. 1906 h c r die Lynplihahnen dcr TTtcrusschlriniliarrt ~viihrcnd der
Scliwangerschaft. Arch. f . Oyn., vol. 7 7 , pp. 1-20.
~ ~ J C K E LA.
,
362
G. B. T$'ISLOCIiI
A N D E. TiT. DEMPSEY
THORN,G. W., AND G. A. HARROP1937 The 'eodiuiii retaining effect' of the
SPY horiiio~ies. Science, vol. 86, pp. 40-41.
TVIsLocKr, G. R., A N D G. L. STREETFX1938 0 1 1 the placentation of the macaque
( Macaca inulatta), f r o m the time of implantation until the formation
of the defiiiitire placenta. (h'negie Contrib. Embrgol., vol. 27, pp.
1 66.
PLATE 1
CSPLBK'ATION O F F I G U R E S
10 Photograph of a 1iistologie:il srction of the muscularis of the uterus taken
froin the spoeimeii f r o m nliicli figure .imas drawii. The lyi~iphatiminjected with
ink are seen intcrizea\iiig with the iiiusclc Iiundles and blood vessels. X 24.
the large lgmph cha~nicls
11 A photograph of the pregiiant uterus slio~\~ing
filled with ink in the deeper p a i t of tlie decitlua. Coinpare this picture with
figure 8. Notice that besides the l~rnplinticsthere arc other clefts, lisible above
in the figure, which are uniiijected. These are thcx flatteiicd luiiiens of uterine
glaiids. X 2cf.
1 9 A section through tlir v:igin:il ~ v a l lof :I rlicsii~niolikey 011 the t\\enty-thiril
(la>*of cycle, showing 1>mplintic~in the tiiuira propria. Coinpare with figure 4
\\+iicli is from tlie same speeiincii. x 20.
I 3 A seelion thiongli the scxii:il skin slioning the 1yiii~)liatic.siii tlie coriiiin.
This a n d figure 9 :ire froin tlic s:iiiic sprciiiieii, ol)tainccl fro111 a 1)regnaiit animal.
x 24.
14 Photograph of a stained, thick section of the xagina illustrating the
lpnqiliatir plexus iii the tuiiica liropria. Same jii\ciiile rliesus monkey as in
figures 1 , 2 a n d 3. X 24.
LYJIPIL2TICS O F l!E;\IALE
RBPRO1)UCTIVE TRACT
0. B. WISLOCKI A N D 1. W . D E M P S E Y
363
PLAT13 1
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