Paper - A study of the structure and vascular conditions of the human corpus luteum in the menstrual cycle and in pregnancy

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Ninian F. A study of the structure and vascular conditions of the human corpus luteum in the menstrual cycle and in pregnancy. (1933) Irish J. Med. Sci. 8(1): 1-16.

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Note this historic paper was published in 1933 and our understanding of corpus luteum development has improved since this historic human study.


See also by this author - Ninian F. Circulation of the maternal blood through the placenta. (1939) Irish J. Med. Sci. 14(2): 59-65.


Modern Notes: corpus luteum

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A Study of the Structure and Vascular Conditions of the Human Corpus Luteum in the Menstrual Cycle and in Pregnancy

By Ninian Falkiner.

(1933)


Introduction

The changes that characterise the endometrium during pregnancy and the menstrual cycle have been extensively studied and well understood since the initial work of Hitschman and Adler on the menstrual cycle. Two outstanding features characterise the endometrium in the menstrual cycle, namely, the secretory activity of the glands and the haemorrhage of menstruation, which occurs at about the time the secretory activity ceases. The behaviour of the endometrium or decidua in early pregnancy contrasts with what happens in the menstrual cycle, for the secretory activity is maintained. Any hmmorrhage that occurs is localised and due to the activities of the trophoblast and does not occur generally through the mucosa as it does in menstruation.


It was natural to ascribe very important functions to the corpus luteum in its relationship to both the menstrual cycle and the phenomena of early pregnancy, for its degeneration in the former cycle and its persistence during pregnancy had long been recognised. The difierences, however, between the corpus luteum of the menstrual cycle and the corpus luteum of pregnancy are not very definitely described in textbooks of gynaecology and midwifery. A corpus luteum of pregnancy persists for many months, while the corpus luteum of the menstrual cycle has only a short period of activity — some 14 days, more or less.


Should menstruation occur (in the absence of fertilization), there is no doubt that the corpus luteum will degenerate; should pregnancy occur, there is no doubt that the corpus luteum will be given a new lease of life and persist for many months as an active structure.


Now it will be readily seen that to compare a corpus luteum of menstruation to a corpus luteum of pregnancy is like the comparison of a young creature to an adult of the same variety, but that to compare the corpus luteum of menstruation during its degenerative stage, namely, actually just before and during menstruation, to the corpus luteum of very early pregnancy is to compare structures of the same age undergoing very different changes and affords a logical basis for sound conclusions.

There seems to be a good deal of uncertainty about the actual histology of the corpus luteum from its formation to its degeneration in the menstrual cycle. In Obstetrics, Williains‘ does not definitely state either the time or the nature of the crst degenerative changes in the corpus luteum of the menstrual cycle. Its period of greatest development, however, is said to occur 14 days after rupture of the follicle.


The occurrence of hmmorrhage at the time of ovulation accounts for a central blood clot in most human corpora lutea, but it is not a constant factor. Williams does not mention the occurrence of haimori-hage at any other period of the development or regression of the corpus luteum.


In Gynaecology, Graves‘ gives a very good account of the physiology of the uterus and ovaries; in it he states that, contrary to the general belief, hmmorrhage does not as a rule take place into the cavity of the follicle at the time of rupture.


It is remarkable that two such authorities as Williams and Graves should differ over the very beginnings of the corpus luteum. It is not, however, a matter of very great significance; apparently haamorrhage at the time of ovulation is likely to occur and indeed may assume grave proportions. Graves states that haemorrhage does not occur during the proliferation and that it may be renewed during the menstrual period. He states that after the corpus luteum has reached its height of development and after menstruation takes place it enters the stage of retrogression. Such a statement implies that the corpus luteum does not commence to degenerate till after the onset of the menstrual period.


It is interesting to note the absence of data in respect to corpora lutea depicted in illustrations in textbooks. They may be either from pregnancy or the menstrual cycle, but no information is considered necessary or advisable.


In developmental anatomy, Arey’ quotes Aschoff as stating: “ There is little or no bleeding into the cavity at the time of the collapse of the follicle, the significant amount of blood appears later at the next mounts.” The recognition of bleeding at the time of the onset of the menstrual flow as taking place in the corpus luteum seems a most important observation, but Aschoff ’s findings do not appear to have aroused general comment in textbooks of midwifery or gynaecology.


In their Short Practice of Gynaecology, J ellett and Tottenham‘ recognise the occurrence of hsemorrhage at ovulation, but definitely place the onset of regression in the corpus luteum to the middle of the ensuing cycle. The differentiation between the corpus luteum of pregnancy and of menstruation is referred to thus:

“ In the corpus luteum of menstruation there is a considerable escape of blood into the lumen; the connective tissue membrane between the lutein layer and the lumen is poorly marked and no colloid or calcium can be found. In the corpus luteum of pregnancy there is usually no blood in the lumen, the contents of which are more organised, and there is an abundant colloid during the first half of pregnancy and frequently calcium dfuring the iecoiid half. It is also usually larger than the corpus luteum of menstruation.


Solomons‘ gives a good account of the changes that take place in the corpus luteum, and recounts the various stages, namely, of proliferation, vascularisation, maturity, and retrogression. In describing the fourth stage, he uses the following words :——“ When menstruation occurs, the corpus luteum becomes filled with blood and retrogresses. ’ ’ He recognises the occurrence of bleeding at the time of ovulation. His account includes clear illustrations of the component cells of the ripe follicle and the corpus luteum.


The best account of the corpus luteum in the literature I have consulted is given by Novak‘. Here are incorporated descripti-ons of the follicle from its rupture till the corpus luteum fully develops. Although not stating very definitely in the text that hemorrhage occurs in the corpus luteum at the time of the onset of the menstrual flow, a quotation from Narcotty is given which leaves the impression that such bleeding is believed to occur.


From the foregoing it will be seen that there is no uniformity of opinion as regards the actual time or nature of the degenerative changes occurring in the corpus luteum, but it is evident that hmmorrhage characterises the structure at certain stages of its existence.


Hartman has contended that there is an active substance originating outside the ovaries that causes the periodic bleeding which we call menstruation. He announces, on experimental evidence, that it is the anterior pituitary that elaborates the substance causing uterine bleeding. Granting that his conclusions are sound, it would seem to me that coincident haemorrhage in both the endometrium and in the corpus luteum might occur, as in each structure there are newly formed blood vessels, capillary in nature, and if a substance produces hmmorrhage in one it is likely to do so in the other.


With the intention of producing evidence bearing on this particular aspect of the sexual cycle in the human female I have, when possible, resected corpora lutea in various phases of the cycle and in cases of pregnancy, in each case using the utmost care to avoid trauma to the delicate structure and ensuring good fixation by at once placing specimens in the fixative agents.

Description of Material

The series comprises a number of corpora lutea, seven of which I will describe. They were removed on the 14th, 25th, 27th, 1st and 3rd days of the cycle ; two are from pregnant cases terminated five days after the first missed period and 56 days after the first missed period respectively. Thus if, for the sake of argument, one adopts the 14th day as the average date of ovulation, we have a series comprising a very young corpus luteum, one of 11 days, 13 days, 15 days, 17 days of the menstrual cycle, one of 19 days and one of 70 days of pregnancy. In only one case did a bimanual examination precede the operation on the previous day.

All the other cases had been examined some days or weeks previous to operation, but the detailed notes of each case will precede the description of each specimen. This is of importance,


Fig. 1. Corpus Luteum. 14th day of cycle (ir1'egu]a1'). showing stigma 111a1'ked S and collection of eXt1'-mrasated blood marked B. The blood is situated in the central cavit-‘V and occupies the part of the cavity proximal to the stigma. (X 7.)

II.

Corpus Luteum. 27th day of cycle (28 day). This corpus luteum shows no gross haemonhage i11 its central Cavity. The mass marked L is :1 tongue of luteal tissue projecting into the Cavity. (X 7.)


for I have noted in cases that have been examined just prior to operation that the corpus luteum has been the seat of trauma. History of first Specimen.

No. 7749. iii. 20. Examined-—-19. 7. ’32.

Age 18. Unmarried. Menstruation irregular but as a rule 28 day interval.

Symptoms--Pain in the left side.

U terns normal in position.

Operation — 3. 8. ’32 (14th day of cycle). Laparotomy.

findings-—-Retrocsecal appendix showing signs of recent inflammation. Appendicectomy. Corpus luteum resected from the left ovary. Bleeding or menstruation occurred within 48 hours of the operation.

The Specimen.

Maeroscopically the section through the meridian of the corpus luteum showed a very definite stigma.

The measurements after fixation were 2.0 ems. by 0.9 cm.

The history and the appearance of the corpus luteum suggest that ovulation had preceded the operation by a comparatively short period, possibly two days or less.

Apparently a resected corpus luteum separates from the ovarian tissue, carrying with it both the theca externa and the theca interna.

This is certainly the case in this specimen and in other corpora lutea that I have resected.

In figure I, a microphotograph (x 7), depicts the general characteristics. At this magnification, the main features recognised are :---—

1. A central cavity occupied by a clear coagulum at the pole further from the stigma marked S.

A collection of extravasated blood occupies that part of the cavity near the stigma.

Although this blood extravasation is most marked at this part uof the cavity, small quantities are seen contiguous with the inner ‘limits of the luteal cells.

2. The luteal tissue is not markedly folded and thus varies greatly in depth. Its inner margin is somewhat irregular, a feature more easily recognised at higher magnification.

Under a high magnification, further features are revealed. The cells of the theca interna are easily distinguished and lie in irregular wedge-shaped masses amongst the luteal cells which are larger and show varying degrees of vacuolation.


Tracing the theca interna cells towards the centre of the corpus luteum, it becomes increasingly difficult to identify them. The luteal tissue is vascularised to a great degree, but not completely, and where the luteal cells are contiguous with the central cavity, there is, at some places, no connective tissue limiting their border. In the main, however, there is a definite layer of loosely arranged connective tissue cells bordering the internal surface of the luteal cells and separating it from the central cavity.

A remarkable feature of these cells is their arrangement into centripetal strands, especially where they are in contact with the blood extravasation.

In the cytoplasm of such cells, small granules of blood pigment are seen.

Summa.ry.—This is a very young corpus luteum, as instanced by the incomplete development of its fibrous and vascular structure. The degree of vacuolation in the luteal cells suggests an already active function. The extravasated blood is in all probability derived from the vessels traumatised at ovulation, but the distribution of the blood around the margin of the central cavity is possibly the result of hwmorrhage arising from the vessels of the theca interna. Williams‘ regards this latter source as the most important. Novak°, however, does not‘ confirm Williams’ opinion.

Second Specimen.

No. 100. iii. 42. Examined——-29. 4. ’32.

Age 34. Unmarried. Menstruation regular, periodicity 28 days.

Symptoms—-—Pain in the back.

Physical sig*ns-———Retroversi,on of the uterus.

0pemtiovn.——9. 5. ’32 (27th day of cycle). Appendicectomy, Gilliam suspension. Corpus luteum resected.

Specimen fixed in Da Fano"s solution.

Measurements of approximately meridian section, after fixation, 1.8 cms by 1.2 ems.

The removal of this corpus luteum was followed by the onset of menstrual bleeding on the following day. figure II is a micro photograph (x 7) depicting the general characteristics of this specimen.

The main features to be recognised are :— , 1. A central cavity occupied by a clear coagulum in the midst of which there is situated a curious tongue of luteal tissue which is really contiguous with the rest of the luteal cells (fig. 2. L.T.), but projects into the cavity in a remarkable fashion. 2. A fairly even layer of luteal tissue, averaging about 2 mm. in depth and presenting a moderately folded appearance, especially at the lower pole in the illustration.

3. The connective tissue strands amongst the luteal cells and bordering their internal limits is well marked. This latter layer dividing the luteal cells shows up as a dark line. This is due to two factors, (a) the deep staining of the connective tissue cells, and (b) the presence of a moderate amount of red blood cells which are possibly already extravasated.

The high power reveals a very definite differentiation of the theca externa from the theca interna. The former is congested and vascular. The cells of the latter are well shown by virtue of their argentophil tendencies and are seen distributed amongst the luteal cells. The luteal cells are vacuolated, but not to such a marked degree as in the specimen just described.

Summary. — In this corpus luteum there is no gross hamorrhage fiG. III. 25t1_1 day of cycle (i1-regular, Va1'_ving from 26 days). The congestlon m the vessels of the luteal tlsslle 15; well

Shown and at the 111:11*gi11 of the luteal tissue where it ho1‘der.<4 the central cavlty extravasatlon of blood has C-0n1me11ce(1_. (x 7.)

Corpus Luteum.

fiG. IV. Corpus Luteum. 1st day of menstruation. The central cavity IS oocupled by blood (B). The luteal tissue is anselmc. (x 7.)


although scattered through the cavity there are small collections of red blood cells.

The luteal cells are well differentiated from the theca interns. cells by the nature of the fixation.

The connective tissue is well developed, in contrast to the last specimen described.

In the connective tissues there is either congestion or very moderate extravasation of blood.

Third Specimen.

No. 7603. iii. 93. Examined—8. 6. '32.

Age 39. Married. 5 para. Periodicity irregular, varied between 26 and 31 days.

Symptoms——Prolapse of the uterus.

Physical signs - Prolapsed uterus enlarged and retroverted.

Operation ~—9. 6. ’32 (25th day of cycle). Abdominal hysterectomy.

The specimen is deliberately described after the previous one although the actual age in days is possibly younger. The reason for this is that the uterine mucosa shows an immediately premenstrual condition, not only with regard to commencing blood extravasation in the stroma, but also with regard to the gland picture and the appearance of the individual cells of the stroma.

I am not absolutely satisfied to take this specimen in itself as very good evidence of the appearance of the corpus luteum just before the onset of menstruation, but I have another specimen obtained on the 30th day of the cycle (menstruation had not yet occurred), whose appearance is very similar.

The histology, however, of this specimen is very striking and the reader can criticise the conclusions, as all the facts are before him, including the important evidence that a bimanual examination was made 24 hours before operation.

Specimen. .

Size-—-1.7 ems. by 1.4 cms., after fixation.

figure III is a microphotograph (x 7) of this specimen. In it will be seen a central cavity occupied by a clear coagulum. The luteal tissue is somewhat more folded than in the previously described specimens and its average depth is greater, up to 4mms. The most obvious feature to be seen in the photograph is the amount of congestion in the vessels, not only of the theca externa but of the capillaries in the luteal tissue and in the connective tissue between the luteal tissue and the central cavity. This condition of congestion compares most interestingly with the endometrium.

Again, in this specimen the theca interns and externa are easily distinguishable, the cells of the latter forming characteristic wedge-shaped masses between the folds of the luteal cells, and the whole structure is very well vascularised and has a complete stroma. of connective tissue which includes a well defined layer between the luteal tissue and the central cavity.

Summary: - This corpus luteum, which I conclude is removed HUMAN CORPUS LUTEUM ‘ 7

just before the onset of menstrual bleeding, shows very marked congestion and commencing haemorrhage in the area between the luteal cells and the central cavity, but as yet the blood has not burst its way into the central cavity to any marked extent. The number of luteal cells, or rather the mass of luteal tissue, appears greater than in the two previous specimens, but vacuolation of the cells is less marked than in the first specimen described.

Fourth Specimen.

No. 7450. iii. 11. Examined—31. 3. ’32.

Age 39. Married 10 years. 3 para. Last pregnancy 1926. Periodicity 28 days.

Symptoms--Abdominal tumour.

Physical signs———Tumour reached to ensiform process.

Operat£ow—4. 4. ’32. Total hysterectomy.

The tumour, though very large, was intraligamentary and had not distorted the uterine cavity, and there had been no disturbance of the menstrual cycle. The menstrual fl-ow started the evening prior to the operation. This means that the operation was done in the first 24 hours after the onset of the menstrual flow.

The uterine mucosa presents the following features :-»-The surface epithelium is in most places intact, but there are many areas where it has become ragged and stripped.

There is a well marked compact layer of stroma wherein the individual cells are large, but there is remarkably little blood either extravasated or in the nature of congestion.

The glands present a collapsed condition, as does the ‘whole mucosa in comparison to the mucosa in the previously described specimen.

The corpus luteum measurements of approximately meridian section after fixation are 1.4 ems. by 1.2 ems.

» figure IV. is a microphotograph (x 7) and shows the general characteristics of the specimen.

The central cavity is occupied to a large extent by a clear eoagulum, while at the deeper end of the structure the cavity is occupied by a good deal of extravasated blood. This extravasated blood forms a fairly even layer around the margins of the central cavity. Its position as regards the connective tissue which separates the luteal cells from the central cavity is very definite. It lies in the cavity 0f the corpus luteum.

The luteal cells are not well stained and are smaller than in the previous specimens. There is a good deal of vacuolation of the luteal cells. There is not any congestion of the capillaries that run between the luteal cells, but the vessels in the theca externa are dilated. The staining of the whole section is much less intensive than of the previous specimen.

Summary. — This corpus luteum, removed on the first day of men_struation,. shows an extravasation of blood into the central cavity which is not limited to any part of the periphery of the cavity. The luteal tissue is not well stained and is amemie. silo.

fiG. V. 3rd day of menstruation.

Corpus Luteum. The central cavity IS occupied by blood (B). The lute.-11 tissue is markedly amaemic. (x 7.) fiG. VI.

Corpus Luteum of P1'e'gnancy——obtained 5th day after

missed period. The central cavity is quite free from blood and the luteal tissue is deeply staining and vascular.


The theca externa and theca interna are both well preserved and the cells of the latter are well stained and show up remarkably in contrast to the luteal cells.

The depth of the luteal tissue is less than in the previous specimen. « fifth Specimen. No. 7170. iii. 379. Examined——-14. 11. ’31.

Age 41. Married. 13 years since last pregnancy. Periodicity 21 days.

Symptoms--Menorrhagia.

Physical signs-—Uterus enlarged and cervix unhealthy.

Opemtion-——19. 11. ’31. ‘Total hysterectomy.

The corpus luteum measured 1.0 cm. by 0.9 cm. It is illustrated in fig. V (x 7), and the features recognised are the very pale luteal tissue while the central cavity is occupied by an extravasation of blood which is situated to one side of the cavity.

The photograph accentuates this feature as, on an inspection of the actual slide, the blood is seen to be distributed more widely around the margins of the cavity.

The luteal cells are small and vacuolation is not a marked feature. The cells of the theca interna and the cells of the theca externa are not easy to diflerentiate and there is an infiltration of the luteal tissue with small round cells.

Summary. — A blood clot occupies the central cavity. The luteal cells are badly stained and present a homogenous appearance.

There is a marked anmmia of the luteal tissue, while the individual cells of the theca interna are not easily recognised.

The conditions in this specimen seem to provide a natural sequel to those of the previously described specimen.

Sixth Specimen (No. 99).

This specimen is described in the account of an early ovum in the J o-wmcl of Obstetrics and Gynaecology of the British Empire.‘ It was resected on the 5th day after a missed period and is, therefore, approximately two days older than the previously described specimen. It was fixed in picroformol.

The measurements of this specimen are 1.2 cms. by 0.7 cms.

The depth of the luteal tissue is very even and measures 4 mms. , figure VI is a microphotograph (x 7) diameters.

The central cavity is rather collapsed. In it there is no gross heemorrhage. There is more connective tissue in the central cavity than in any of the previous specimens. The border of connective tissue between the luteal cells and the central cavity is well defined. The luteal cells are well stained and the vascular

channels are shown up by the deep staining of their walls, although there is no congestion.

There is a good deal of vacuolation.

The theca interna cells are beautifully differentiated, while the theca externa is well marked and vascular.

Summary. — This corpus luteum shows no gross hmmorrhage in its central cavity, although small collections of blood cells can be recognised.

The central core is markedly fibrous and the general appearance of the luteal tissue suggests continued activity.

Seventh Specimen (No. R 1).

This corpus luteum was removed in the course of a hysterectomy during pregnancy in the case of multiple fibroids, the size and the position of which precluded the possibility of the continuance of pregnancy or a conservative operation. (The patient was suffering from acute intestinal obstruction due tosimpaction at the time of operation.)

I am indebted to the Master of the Rotunda Hospital for the opportunity of describing this specimen.

The pregnancy had lasted 84 days since the last period, so the age of the corpus luteum may be calculated as about 70 days.

The corpus luteum was fixed in formalin and the section measures 2 cms. by 0.7 cms.

Its appearance is illustrated in figure VII, where it is magnified by 7 diameters.

This picture shows the general structure very well, and the central cavity is occupied by firm fibrous tissue. The cavity has collapsed since fixation and apparently contained a cystic centre.

There is no trace of hmmorrhage in this specimen.

The luteal cells are well stained and vacuolation is well marked.

The endothelial walls of the capillaries in the luteal tissue are well stained and there is no congestion.

The theca interna cells are well differentiated while the theca externa is very definite and shows up as a well stained and vascular area.

Summaxry. - This corpus luteum shows no hmmorrhage either macroscopic or microscopic.

The luteal tissue is bulky and well vascularised.

The connective tissue is more fully developed than in any of the previous specimens and all the constituent cells are well differentiated.

Comparing it with the corpus luteum of pregnancy previously described, it is larger and its individual luteal cells are not so well stained.

Discussion

In the sixteenth century the corpus luteum was recognised, and was accurately described by.Ma1pighi in 1689 and given its name by that writer.

In its highest form of development the corpus luteum is essentially a mammalian structure, but is particularly well developed in the monotremes, which differ from the higher mammals in being oviparous. In the amphibia the cells of the egg follicles persist for some time after ovulation, and in the reptilia they actually hypertrophy to some extent.


Fig. VII. Corpus Luteum 01' P1‘e,q,m1ncy—-—0b’mi11ed after missed period. The ce11t1'a1 cavity contains no blood and the luteal tissue is well stained and vascular.

Fig. VIII. The haemorrhage depicted in black is seen in the region of the stigma, from the margins of which it is presumed to have come at the time of ovulation. This corpus luteum shows very moderate folding because it was removed so soon after ovulation.

The corpus luteum shows very even folding and no haenlorrhage. This condition is associated with the active functioning of the structure.

Later, the corpus luteum becomes associated with lactation and with the imbedding of the ovum in the uterine mucosa.

Many problems regarding both the function and structure of the corpus luteum have been solved in the last few years, and S. A. Asdell“ contributed a full review of accepted work in 1928. From his article I have derived many references in the subsequent text. The first suggested function to withstand criticism was made by Beard in 1897. He stated that the corpus luteum was responsible for the suppression of ovulation during pregnancy. A great deal of experimental work supports this theory. Born and Fraenkel were the first to recognise a relationship between the nutrition of the embryo and the secretion of the corpus luteum. There is no doubt that the corpus luteum has very great influence during the early stage of pregnancy, particularly with the imbedding of the ovum and its subsequent nutrition. When imbedding is completed, however, the influence of the corpus luteum on the subsequent welfare of the pregnancy diflers in different species of mammalia.


In the duckbill platypus, where imbedding does not occur, the corpus luteum is a well marked structure. Its functions may have to do with the welfare of the embryo between the time of fertilisation and the laying of the egg. Placentation differs tremendously in different mammalia, and I believe that the structure and life history of the corpus luteum bear some relationship to placentation. When one realises, however, the very complicated factors that influence placentation even in closely allied species, the solution of this relationship becomes a most baffling problem. I believe that Grosser’s” classification of placentae provides the most convenient when the purpose in hand is to co-relate conditions in the corpus luteum to those in the uterus, both in the absence and the presence of pregnancy. His classification depends on the degree of intimacy that is established between the foetal tissues and the maternal tissues, thus, placenta epithelio-chorialis in the ungulates, where the chorion does not do more than make close contact with the epithelial lining of the uterus.


A further stage of invasion is reached in the ruminants where the chorionic epithelium gains contact with the connective tissues of the uterine mucosa and the placenta is then termed “ placenta syndesmochorialis. ” In the carnivora, the chorionic epithelium comes in contact with the endothelium of the maternal vessels and this condition is termed “ placenta endotheliochorialis.”

In the primates, the chorionic epithelium actually invades the maternal vessels, and this produces a placenta “ haemo-chorialis. ”

Such a classification of placenta; certainly gives a very clear insight into the mode of transference of nutrition from the maternal organism to the foetus.

Huxley“ had introduced in 1864 a classification of placenta in which the mammals were divided into two great groups, the deciduate and non—deciduate.

This classification depends upon the degree of participation that HUMAN CORPUS LUTEUM 11

uterine mucosa takes in the formation of placenta. It did not prove satisfactory on account of the fact that it did not take into account the part played by the trophoblast.

Assheton,” to overcome the difficulties, divided placenta into two groups, viz., cumulate and plicate. The main characteristics of the cumulate placenta are as follows :-—

Great radial proliferation of the trophoblast, great destruction of the maternal tissues resulting in bleeding, degeneration of the uterine glands with consequent cessation of their secretion as supplying embryotrophe to the foetus.


The main characteristics of the plicate placenta are as follows :-— Great tangential proliferation of tho trophoblast, little destruction of maternal tissue with little or no bleeding, maintenance of the uterine glands throughout pregnancy uith the secretion of importance as embryotrophe.


The fatal conformation of the placenta is very varied, and is probably more important from the purely scientific point of view with regard to the classification of mammals.


Thus we see in the opposum and allied . creatures placenta developed from yolk sac. Such placenta are simple in their structure and in their attachment to the uterus and pregnancy is short-lived as the immature foetus at birth is promptly transferred to a specialised pouch where it is nurtured until it can fend for itself. Ascending in the mammalian scale, we find the yolk sac fading in importance and the omphaloidean placenta being replaced by allantoidean vascularisation of the chorion.


The degree of invasion of the maternal tissue, however, does not advance pare? passu with the alteration in the foetal constituents of the placenta. Thus in the ungulates, a placenta of the allantoidean type is developed with an attachment of the epitheliachorialic description while, in the insectivora, we find in the Erinaceus europclms, in the early stages of pregnancy, a yolk sac placenta which is replaced by an allantoic placenta as pregnancy advances. Yet the attachment to the maternal tissues in the hedgehog placenta is much more intimate than in the ungulates.

In summing up the function of the corpus luteum with regard to implantation and gestation, Asdell“ states :—

“ As things stand at present,’ one must conclude that early removal of the corpora lutea prevents the continuance of pregnancy in all species except the guinea pig, but that in the rodents, at any rate, removal may not always be followed by destruction of the foetus. In view of these results, it is impoible to come to any definite conclusion applicable to all mammals.”

A consideration of the type of placentation, however, in conjunction with a consideration of the result of removal of the corpus luteum, may provide a suitable basis for conclusions.

In the rabbit, the results of removal of the corpus luteum were constant in causing termination of the pregnancy, according to Frankel.

The removal of the corpus luteum in 48 cases before implantation, 19 cases in the first fortnight of pregnancy and in 51 cases .


fiG. XI. Represented here is the condition at the onset of the 1116-11st1'ua,1 flow, na111ely, haemorrhage mto the cavity of the corpus luteum.


The condition of vascular ellgorgement is illustrated here and the co1nn1e11c1ng extravasatlon of blood Into the central cav1ty. figs. XII, XIII and XIV are adapted from _Anclerse11’s illustrations of the blood supply of the corpus luteu111 i11 the sow. Here they are used to illustrate 111 fig XII the normal blood supply of a fold of luteal tissue in the fully formed structure.

In fig. XI11 the condition of engorge111ent as seen in the specimen illustrated in fig. III is depicted (just prior to the onset of menstruation).

In fig. XIV the occurrence of hsemorrhage into the ca1'it_v of the corpus luteum is shown with the resultant collapse of the vessels 111 the luteal tissue.


in the latter half of pregnancy, resulted in termination of the pregnancy. The duration of pregnancy in the rabbit is 32 days.

Niskobina found that destruction of the corpora lutea in the rabbit was without eflect after the 14th day of pregnancy.

The most frequent finding in cases of excision of the corpus luteum in the rabbit is discontinuance of the pregnancy.

The placenta in the rabbit may be classified under the heading of deciduate, and it comes under the heading of cumulate placenta as described by Assheton. The intimacy between the chorion and the maternal tissues is eventually very complete and results in placenta hmmo-chorialis.


According to Marshall,“ at the end of pregnancy the maternal placenta consists almost entirely of blood and blood symplasma, except for a thin rim of tissue containing blood sinuses at the zone of separation. Marshall states that in the rabbit the glandular secretion is less important than in the dog.


Apparently the blastocyst in the rabbit does not imbed as rapidly as that of the guinea-pig, which approximates more closely to the human ovum in its behaviour after it enters the uterus. Von Spee has shown how very rapidly it gains an interstitial attachment to the uterine mucosa.

The findings as regards the removal of the corpus luteum in the guinea-pig during pregnancy do not suggest that the corpus luteum is necessary to the continuance of pregnancy in this rodent. _

Removal of the corpus luteum in early pregnancy in bitches caused termination of the pregnancy in the first four weeks of pregnancy. (Marshall and Jolly).

There is no doubt that removal of the corpus luteum in the pregnant human female has not been constantly followed by termination of the pregnancy. Cases have been reported (Corbet“), from as early as the first month in which no disturbance has occurred following the removal of the corpus luteum.

Results are always open to criticism from the point of view that some luteal tissue may have been left or, on the other hand, results which include termination of the pregnancy may be criticised from the point of view that the operative interference apart from the removal of the corpus luteum has caused the termination of the pregnancy.

There are, however, too manycases of continuance of pregnancy in the human female after the removal of the corpus luteum to neglect the import of such results.


The continuance of pregnancy after the removal of the corpus luteum is far more significant than its termination, for it means that the corpus luteum is not essential to the welfare of the foetus. The results of Drummond Robinson and Asdell, working in goats, have been constant in that removal of the corpus luteum has always resulted in the termination of pregnancy at all periods of gestation.


In the ungulates, the attachment at the ovum is centric and the type of placentation plicate or, according to Grosser ’s classification, placenta epithelio-chorialis exists.

Thus we see that there are constant results in this type of placentation, while in pregnancy in the carnivora and rodents results are not constant, and similar findings (not constant) exist in the human female.

Thus in the mammals as a general rule we find, ascending in the scale, a lessening tendency to abort, when the corpus luteum is removed, as placentation increases in complexity. This finding is altogether in keeping with what we do know of the relationship of corpus luteum activity and the secretory activity of the uterine epithelium.

The human female bleeds under physiological circumstances, while the occurrence of hamorrhage in the male is always (as far as I am aware) pathological.

The physiological haamorrhages in the human female occur at menstruation from the uterine mucosa, at the time of nidation of the ovum (these are microscopic bleedings and do not normally become recognisable), and at delivery, the separation of the afterbirth is always accompanied by bleeding. All these haemorrhages occur from the lining of the uterus and, in addition, there are, if my thesis is correct, physiological haemorrhages in the ovary, both at ovulation in the follicle and at the time of onset of the menstrual flow in the corpus luteum.

All these hmmorrhages may be classified as being either traumatic or due to some internal secretion.


This aspect of the haemorrhage in the human female has not received sufficient attention, for it must be remembered that the pathology of reproduction includes many conditions in which hwmorrh age is an outstanding characteristic. It is, therefore, most important to understand the nature of the physiological bleedings in the human female.


My point is that where the termination of pseudo-pregnancy is associated with haemorrhage in the uterine mucosa and the corpus luteum it is then an index of the preparations that have been made for a placentation involving an interstital imbedding associated with complete invasion of the vascular components of the endometrium.


Apparently in the human female there is not only haemorrhage in the endometrium at the onset of menstruation but, in addition, bleeding occurs in the corpus luteum.

Summary and Conclusions

In order to present clearly the interpretation of the series of corpora lutea that I have described, I have had diagrammatic pictures drawn of the various specimens from the menstrual cycle. (I did not consider that the specimens of the pregnancy corpora lutea needed further explanation.)

In the first of these drawings, fig. VIII (adapted from fig I), the luteal tissue is not markedly folded and it is interesting to note that this folding of the luteal tissue depends on two factors: the increase in size of the individual luteal cells—(authorities agree that there is no proliferation of these luteal cells although it is diificult to believe that the granulosa layer of the follicle contains as many cells as are present in a mature corpus luteum)-— and, secondly, the invasion of the luteal tissue by the connective and vascular elements of the thecen.

The blood in the interior is shown distributed mainly at the pole of the corpus which is near the stigma.

Another point illustrated very clearly is the apparent (but not real) uneven thickness of the luteal tissue, and this perhaps is due to the fact that parts of the corpus luteum may be vascularised before others.

Corner" has noted in a sow that the discus proligerosus is actually vascularised to some degree before ovulation.

The next figure, fig. IX (adapted from fig. II), differs slightly from the actual section that it is representing. The tongue of luteal tissue is omitted as its inclusion complicates the diagrammatic efiect that I wish to present in these drawings.

This drawing shows the very perfect organisation of the corpus luteum, its perfect fibrous capsule indicating a complete vascularisation, and such a structure is well adapted to be a gland of internal secretion.

This picture to my mind presents the fully developed corpus luteum of the menstrual cycle and its further development as a corpus luteum of pregnancy might be possible in the event of fertilisation.

The next drawing, fig. X (adapted from fig. III), presents .a picture of extreme congestion, and here, as in the previous specimen, the folding is very remarkable.

The vessels bordering the central core are congested as well as those in the luteal tissue. .

This picture presents to my mind a condition of vascular degeneration from which there is no return and must merge in to the condition of hemorrhage illustrated in the next diagram.

The following diagram fig. XI (adapted from fig. IV), illustrates the haemorrhage having occurred and the blood has made its way into the central cavity. The effect of such a rupture in the vessels of the corpora lutea of menstruation must be to interrupt the circulation through this little gland of internal secretion to an almost overwhelming extent. Thus the progestin delivery to the blood stream is instantaneously reduced to a minimum and the condition of the appearance of the luteal cells after this haemorrhage has occurred can be little or no index to their physiological efficiency when their circulation is so interfered with.

In order to illustrate diagrammatically the vascular conditions of the corpus luteum, I have utilised and adapted the illustrations of Andersen,“ which were derived from investigations of the injected corpus luteum of the sow.

Each fold of the corpus luteum represents to my mind a complete entity in that it contains a vascular supply consisting of a small arteriole and a vein with capillaries circulating amongst the luteal cells. Each fold is in itself complete and the changes illustrated for such an entity give a true index of the condition of the gland as a whole.


The first illustration, fig. XII, of this group shows the capillaries in their fully developed condition ramifying among the luteal cells and reaching right up to the limits of the lutcal tissue where it is bounded by a connective tissue capsule which separates it from the central core. The second illustration, fig. XIII, shows these capillaries dilated as they are immediately preceding the onset of the menstrual flow. The third shows them collapsed, fig. XIV, with their terminal branches ruptured where they are unsupported and bordering on the connective tissue which separates them from the central cavity. The blood has escaped from them and is lying in the cavity of the corpus luteum. I feel that these illustrations show very clearly what my interpretation of the series of specimens under consideration means. I do not think, from a study of the sections, that the vascular arrangement in the human corpus luteum diflers much from that existing in the sow.

Conclusions

1. That in mammals in which there exists a placenta hemochorialis, the most important subject for consideration both in the uterus and corpus luteum is the vascular arrangement. (It will be remembered that the condition of the glands of the human uterine mucosa, though histologically presenting the most obvious constituent, has gradually faded in importance as an index of the pathology of the endometrium. This is not a matter of surprise when a consideration of the symptomatology of uterine disease is made; the main symptom is hsemorrhage).

2. That hemmorrhage occurs in the corpus luteum at two different stages of the menstrual cycle.

The first hmmorrhage occurs at the time of ovulation and according to authorities is very variable in amount, its actual occurrence being doubted by many. This haamorrhage is traumatic and localised. The second haemorrhage occurs in or about the time of the onset of the menstrual flow, and is generalised throughout the terminal capillaries which border the connective tissue dividing the luteal cells from the central cavity.

The recognition of haemorrhage in the corpus luteum during its formation has been alluded to by many. I believe that such haemorrhage may be discounted, as its causation has probably been the trauma incident to the removal and handling of an organ in such a delicate vascular condition.

3. That when hemorrhage occurs in the corpus luteum, it marks the end of its career as a gland of internal secretion, as the resultant disturbance in the circulation precludes the possibility of an uninterrupted circulation through the structure which, of course, must be regarded as a necessity for the transference of the internal secretion to the other organs of the body.

4. That when pregnancy supervenes, no hmmorrhage intervenes and the corpus luteum persists as an active organ of internal secretion. To what period this activity is prolonged in the human female must remain doubtful. My belief is that if the number of cells in the corpus luteum is incapable of increase that the secretion is prolonged until the individual cells become senile; so that there is a gradual withdrawal of secretion in the human female which probably ceases to be of importance as early as the second month of pregnancy.

5. That the recognition of contemporaneous hwmorrhage in the uterine mucosa and in the corpus luteum will become recognised as investigations are made on series of corpora lutea from the menstrual cycle and pregnancy. That such a recognition will lend support to Hartman ’s work which has already done much to straighten out the difficulties of a complete understanding of the menstrual cycle in the primates.

6. That the present series is small and, therefore, not suificient to allow the formation of conclusions immune from criticism and elaboration. But that care has been taken, in the collection, as regards the history and fixation of the material and no specimens have been discarded on account of not fitting in with the ideas that promoted the investigation.



My thanks are due to Professor Wigham, in whose department the sectioning of most of the material was carried out. I also wish to thank Professor Gatenby, who has allowed me to work in his laboratories and to consult the literature that he has collected on the subject. Miss Mairin 0’Brien has taken the greatest trouble with the drawings and I fully appreciate the value of her work. I am indebted to Professor J. P. Hill for the photographs, which were taken in the Department of Anatomy, University College, London.

References

Obstetrics. Appleton, New York, 1931.

6. Gynaecology. Saunders, Philadelphia, 1928.

7. Developmental Anatomy. Saunders, Philadelphia, 1930.

8. Short Practice of Gynaecology. Churchill, 1930.

9. Handbook of Gyncrcology. Bailliere, Tindall and Cox, 1925. . Menstruation and its Disorders. Appleton, New York, 1921. . Joum. Obstet. and Gynoec., Brit. Emp., Vol. 39, No. 3, 1932. . Plvysiol. Re'v., Vol. 8, 1928.

10. Manual of Human Embryology (Keibel and Malll. Lippincott, 1910. 10. The Physiology of Reproduction. Longman, 1922.

11. Irish Jowr-n. Med. Sci., Aug., 1932, 520.

12. Amer. Journ. Anat. 1919.

13. Contrib. Embryol., No. 88, 1926.


Cite this page: Hill, M.A. (2019, October 22) Embryology Paper - A study of the structure and vascular conditions of the human corpus luteum in the menstrual cycle and in pregnancy. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_A_study_of_the_structure_and_vascular_conditions_of_the_human_corpus_luteum_in_the_menstrual_cycle_and_in_pregnancy

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