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Lymphology 14 (1981) 17 - 23
The Cyclical Changes in the Uterine Lymphatics of the Pig. Investigations on the Perimetrium*
G. Fabian Department of Anatomy, Ruhr-University, Bochum, W.-Germany
Summary However, up . to the present time little is The orthograde demonstration and outlining of the known (25), about the lymphatic vessels uterine lymphatic system in the pig, during the sexu and capillaries of the u terns although investi al cycle was successfully achieved by the resorption gations in man, domestic animals and in labo of patent blue violet and Japanese ink. During oestrus the lymphatics in the perimetrium ratory animals have enabled further informa are markedly widened and variable in size. tion to be gathered. There have been investi The subsequent phases of the cycle are characterized gations into the lymphatics of the human by a reticulate arrangement so that the preoestrus uterus, also during the recurring cycliCal resembles the picture of oestrus. The removal of the dyestuff takes place through the changes in the uterine mucosa, and even dur myometrium in a matter of seconds into larger ves ing pregnancy (2, 4, 5, 7, 10, 18, 26 , 29, 30, sels in the mesometrium which have a typical bead 31, 32, 33 , 34, 38, 39, 42, 43 , 44, 45 , 46 , ed appearance. 47, 48, 49 , 50, 51 , 54, 55 , 56 , 57 u.a.). In vestigations have taken place into mammalian uterine lymphatics, for example in cattle (3 , Our knowledge concerning the structure and 19, 22, 23, 24, 25), in pigs (1), in horses function of the lymphatic system has been and sheep (21), in cats (27), in rhesus mon greatly enriched during recent decades. The keys (58), in rabbits (35, 52), and in the pure morphological demonstration of the lym mouse (13 , 14, 15 , 16). phatic system has become changed to a func tional morphology of the lymphatic circula In the latter species the investigations have tion (57) and it is only on this basis that any taken place predominantly on the lymphatics pathological occurrence can be understood of the endometrium in young animals up to and explained. the onset of sexual maturity (15), as well as in nulliparous (13) and multiparous (14) ani The first description of the lymphatic system mals in the recognized five stages of the sexu of the uterus was given by Nuck (1692) (37) al cycle, and also in older nulliparous and although the anatomy of the uterus had al multiparous mice (16). ready been described in the first century A.D. by Hippocrates and Galen. Since the time of There have been no reports of similar investi Nuck (37) many research workers have occu gations in the pig, according to the literature pied themselves with this subject and in the which is available to us . In tl1e course of this period that has followed, the angioarchitec research project on sexually mature nullipar ture of the vascular system of the uterus has ous pigs an effort was made to elucidate been investigated in man and other mammals, the cyclic behaviour of the lymphatics in the even during the endometrial cycle. perimetrium during the sexual cycle. *With the support of the , Deutsche Forschungsge meinschaft " (Germ an Research Council)
0024-7766/81 1300-0017 Sl 02.00 © 1981 Georg Thieme Verlag Stuttgart · New York
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Fig. 1 Oestrus. Lymph capillaries in the perimetrium (below) with a larger vessel at the border of the myometrium running in the long axis of the uterine cornu. Absorption of Japanese ink, cleared in oil of wintergreen. Negative magnification 51 x. Positive magnification 288 x
Material and Methods TI1e investigations were carried out on 193 12, 53) as also has Japanese ink (20). The uteri obtained from sexually mature, nulli dye was applied to the surface of the mucous parous pigs (pure-bred German ,Landschwein") membrane of the left cornu of the uterus aged about five months, which were in vari which was opened under the stereo-microscope ous stages of the sexual cycle. As in the pre slightly laterally, by tl1e broad ligament (me vious investigations (13 , 14, 15, 16) patent sometrium). Retrograde and orthograde ·injec blue violet (from Byk-Gulden, Constance) tions of dyestuff were also made. Subsequent was again chosen, because it is known to ly the organ was fixed and put through the have an affinity for the lymphatic system (6, routine histological processes.
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Fig. 2 Early postoestrus. Tortuous reticulate pattern of the lymph capillaries in the perimetrium. Absorption of Japanese ink, cleared in oil of wintergreen. Negative magnification 80 x. Positive magnification 434 x
Results serosal surface). Under the peritoneal surface there appears, plainly outlined a network of The following findings apply to all phases of lymphatic capillaries, which in the further the cycle, the total duration of which is nor course of the removal of the dye subsequent mally 21 days. ly fades away in the direction of the myome After application of Japanese ink to the uter trium. In general it appears that in the sero ine mucosa there appears immediately, on its sal layer (perimetrium), running in the long surface a black pattern which fades away in axis of the uterine cornu, there are two pa to the depths of the mucous membrane and rallel lymph capillaries of larger size, which to some extent can be traced further peripher are joined together by transversely or obliquely ally, that is, towards the perimetrium (the running anastomoses.
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Fig. 3 lnteroestrus. Regularly arranged network of lymph capillaries with dilatations in the perimetrium. Absorption of Japanese ink, cleared in oil of wintergreen. Negative magnification 64 x. Positive magnifi cation 347 x
During oestrus these capillaries in the perime ever, as regards the demonstration of these trium can reach an enormous size, similar to "blind" branches it must be borne in mind those in the endometrium of the mouse (13) that by an appropriate injection of Japanese which, although solitary can reach ten times ink into these blind ends (or beginnings), the size of the predominantly very fine bran lymph capillaries of very fme calibre (l- 6prn) ches which measure up to 3 pm. Coming off are seen to fill. Evidence of this kind can be pro from these branches one can see a larger lymph duced by a similar injection into the subcutane capillary running in the perimetrium to the bor ous tissue of the lower leg in the rat (12). der of the myometrium, in the long axis of the In the next phase of the cycle - early post uterine cornu (Fig. 1). In addition to this a se oestrus - the lymph capillaries are found to be cond lymph capillary runs parallel nearly at the more tortuous and closely packed in their gene base of the perimetrium, which however is only ral appearance. It is the picture of a more uni seen intermittently during oestrus. Both lymph form reticulate character (Fig. 2) whereas the capillaries show a narrow, irregular reticulate pattern of the lymph capillaries in the earlier communication one with the other. phase shows them to be lying relatively close We were unable to demonstrate in this or in together and drawn upwards. the following phase of the cycle, the irregular In late postoestrus the picture changes, to the network with numerous blind ramifications extent that the arrangement of the lymph ca coursing in various ways towards the surface pillaries is much more homogeneous although of the uterus, which had been identified in on account of their great extensibilitY, the the bovine perimetrium by Jel{nek (22). How- capillaries acquire a slightly wavy appearance.
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Fig. 4 Preoestrus. Branches of lymph capillaries visible in the perimetrium (lower part of figure) which are extending into the lymph capillaries at the border of the myometrium and from here are identifiable deeper in the myometrium (upper part of figure). Haematoxylin-Eosin. Negative magnification 160 x. Positive mag nification 867 x
The interoestrus also characterized as the phase myometrium (Fig. 4) in order to joint on of recovery shows the lymph capillaries still to larger lymph capillaries, which in tum slightly wavy but in the form of a uniformly communicate with lymphatics in the myo arranged network. This often exhibits dilatations metrium. at the confluence of several lymph capillaries Finally the removal of the dyestuff from (Fig. 3) similar to the larger lacunae found in here takes place very rapidly (in a matter cattly by Jelfnek (22) in the proliferative phase of seconds) into the mesometrium where of the uterine cycle and also in multiparous the lymphatics have a beaded appearance cattle, and run between the serosa and the blood The preoestrus follows as the last phase of the vessels in the so-called stratum lymphaceum cycle and is continued into the stage of oestrus, (28). in which th"e lymph capillaries in the perimetrium begin to take on an elongated course. Otherwise Discussion it would seem to approach the picture as it ex The perimetrium - the serous covering of ists later in oestrus. That is to say, that the the uterus - is the continuation of the size of the lymph capillaries corresponding double layer of peritoneum which foons the to the interoestrus has increased, likewise broad ligament of the uterus (i.e. the meso there also appears an increase in fine cours- metrium) and it is intimately attached to ing lymph capillaries which seem to be the outer aspects of the myometrium (8). striving to advance to the border of the The wall of the uterus from without in-
Permission granted for single print for individual use. Reproduction not permitted without permission of Journal LYMPHOLOGY. 22 G. Fabian wards consists of the perimetrium, the myo 2 Antipova, E. V.: Ob odvodjascich limfaticeskich metrium, and the endometrium where func sosudach sejki matki i jajicnikov. AkuS. i. ginek. 5 (1963) 82 tionally the most intense changes are found, 3 Baum, H. : Das Lymphgef~system des Rindes. as determined by the sexual cycle. Similar Berlin 1912 fmdings have been recorded in the pig (I 1, 4 Brizzi, E., F. Gasparri: Studio anatomico dei 40, 41) and changes associated with the coUettori linfatici del fondo dell'utero. Arch. sexual cycle have also been demonstrated in ital. anat. Embriol. 67 (1962) 203 5 Bruhns, C.: Ober die Lymphgefai\e des weibli· the blood vessels of the pigs uterus by Enge chen Genitale nebst einigen Bemerkungen tiber mann (9). Investigations have likewise been die Topographie der Leistend.riisen. Arch. Anat. done on the lymphatics (17), in which cycli Entwick.I.-Gesch. (1898) 57 cal changes have been identified in the sepa 6 Byk-Gulden: Personal information 1970 rate phases. Even the perimetrium is involved 7 Cvetkova, A.P.: Vozrastnyje sobenosti limfati· ceskoj sistjemy matki. Ivanovskij med. inst. Sb. in the total processes, as will be shown. naucnych trudov. 23 (1960) 229 Jelinek (22) has undertaken investigations 8 Dobberstein, J., G. Hoffmann: Lehrbuc.h der into cattle, with particular reference to the vergleichenden Anatomie der Haustiere. Bd. 2, lymph capillaries of the perimetrium. If one 2. Autl. S. Hirzel Verlag, Leipzig 1963 uses the metl10d of displaying the lymph 9 Engemann, 1.: Zum zyklischen Verhalten der Gef~e des Schweineuterus. Diss. Berlin FU, capillaries by light microscopy it is to be ex 1969 pected with present day methods, that these 10 Erbsloh, J. : Darstellung des Lymphgef~systems are quite prominent. This has already been der graviden Gebarmutter nach intraamnialer In achieved by the technique employed (12, 13, jektion von Immetal. Zbl. Gynak. 48 (1942) 1911 14, 15, 16) and enabled on to decide whether the 11 Fabian, G.: Zum zyklischen Verhalten vornehm· the removal of the dyestuff takes place through Lich der Hohe des Endometriums beim Schwein. the lymphatics or the veins. In the isolated or Zbl. Vet. Med. 8 (1961) 214 gans which we have been using, removal of the 12 Fabian, G. : Zur Darstellung der Lymphkapilla ren mittels Patentblau-Violett und Tusche. Berl. dyestuff can still be guaranteed more than 15 Miinch. tieriirztl. Wsclu:. 82 (1969) 113 hours post mortem, as a result of the intrinsic 13 Fabian, G.: The Lymphatic Vessels of the Uterus contractility of the lymphatics. Mislin (36) was during the Sexual Cycles of the Mice. Lympho also able to confirm experimentally the inherent logy 9 (1976) 78 (autochthonous) automatism of the lymphatics. 14 Fabian, G. : The Cyclic Changes of the Lymph Vessels in the Uterus of the Mouse which has It is possible to exclude completely any trans been pregnant. Lymphology 10 (1977) 173 port of the dyestuff through the vascular system 15 Fabian, G. : Investigations on the Uterine Lympha· as the contractility of the blood vessels is abolish tics of Juvenile Mice, up to the Onset of Sexual ed soon after death and hence no removal of dye Maturity Lymphology 11 (1978) 123 stuff is possible by this route. It is thus easy to 16 Fabian , G.: Die Lymphgef~e im Uterus alternder nulliparer und multiparer Mause. Lymphologie 3 differentiate the blood vessels from the lymph (1979) 46 atics and lymph capillaries, a point which must 17 Fabian, G.: Die zyklischen Veriinderungen der again be particularly emphasized in these investi Lymphgefa~e im Uterus des Schweines. To be gations. published 1981 18 Gacalov, M.D. : Limfaticeskaja sistema stenki rna· Our fmdings are in agreement with the ob tocnoj truby zensciny. Arch. anat. gistol. embriol. servations of Je/(nek (22) on the lymph ves 35 (1958) 41 sels in the bovine perimetrium and it thus 19 Grigorjev. V.P. : Limfaticeskaja sistjema slizistoj obolocki matkinestelnych korov. Sb. rabot. Le appears that cyclic changes in the lympha ningrad. veterin. inst. 27 (1965) 516 tic system are also demonstrable in the pig 20 Harms, H. : Handbuch der Farbstoffe flir die Mi· in connexion with the sexual cycle. kroskopie. Staufen-Verlag, Kamp-Lintfort 1965 21 Hoggan , G., F.E. Hoggan: On the comparative anatomy of th e lymphatics of the uterus .. J. Anat. References 16 (1881) 50 1 Anderson, D.H. : Lymphatics of the fallopian 22 Jel(nek, K. : Das innere Lymphgef~system der tube of the sow. Carnegie 1nst. of Washington Gebarmutter der Kuh. 1. Lymphkapillaren des Dept. of Embryol. Contr. Embryol. 19 (1927) Perimetrium. Anat. Anz. 138 (1975) 281
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23 Jelinek, K.: Das innere Lymphgef
Priv.-Doz. Dr. Gerda Fabian, Department of Anatomy, Ruhr-University, D-4630 Bochum, Germany
Permission granted for single print for individual use. Reproduction not permitted without permission of Journal LYMPHOLOGY.