Ovulation in the human ovary - Its mechanism and anomalies
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Shaw W. Ovulation in the human ovary - Its mechanism and anomalies. J Obstet. and Gynaecol. (1927) 34(3):
See also by this author - Shaw W. The fate of the graafian follicle in the human ovary. (1925) J. Obst. and Gynaecol. 679-689.
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- 1 Ovulation in the Human Ovary - Its Mechanism and Anomalies
Ovulation in the Human Ovary - Its Mechanism and Anomalies
By Wilfred Shaw, M.A., M.B., B.Ch. (Cantab.) F.R.C.S. (Eng.)
Assistant Professor, Department of Gynaecology and Obstetrics, St. Bartholomew’s Hospital.
The most fundamental of the complex changes which the female generative organs undergo is the process whereby the ripened Graafian follicle discharges its ovum into the peritoneal cavity. The features of the mechanism of ovulation in lower animals can be easily studied, but in Man the only method of obtaining accurate information is to search laboriously through specimens of human ovaries until either a ripening or a recently ruptured follicle is found. As such specimens are rare it is not surprising to find that there is only a small amount of evidence to show the nature of the mechanism in human subjects. It is the purpose of this paper to give an account of follicle ripening and of ovulation in the human ovary and as the former process presents a very common abnormality which leads to the production of an ovarian hzematoma, this condition will also be described.
It has become my habit to deplore our ignorance of the elementary principles of ovarian physiology and there is some justification for this attitude. It is hardly sufficiently emphasized that the reproductive functions are among the earliest properties of cell life to be developed and are responsible for some of the most powerful instincts that dominate the habits of all forms of life. For these reasons it is justifiable to state that probably of all the physiological processes of the body among the most highly specialized and intricate lie the reproductive functions. If these principles were borne in mind the problems of ovarian physiology would be attacked with more humility than is often the case.
In the human ovary at periodic intervals primordial Graafian follicles hypertrophy and become highly specialized in the process of ripening. We are completely ignorant of the factors which determine why this should occur and why only certain primordial follicles hypertrophy, while primordial follicles lying in the immediate vicinity remain inactive. If it is postulated that the activity of a primordial follicle is initiated and controlled by a stimulus, this must be very specific in its action for it selects only a few follicles at a particular time. On the other hand the alternate hypothesis of assuming that the process of ripening begins because an inhibitory stimulus is removed is still more unsatisfactory, for it is difficult to imagine any specificity attached to such a mechanism. From purely theoretical considerations I have indicated elsewhere1 that in all probability the primary fundamental activity of the ovary is displayed in the process of follicle ripening: that this activity has a periodicity constant for the healthy individual and of dimensions which are determined by no known laws and that this periodicity is not inﬂuenced by purely physiological factors. If this hypothesis be accepted it is possible to offer general though by no means detailed explanations of the other functions and activities of the ovaries.
In the process of ripening, quite apart from the changes of maturation of the ovum into which it is not proposed to enter, extremely intricate changes take place. first, there is considerable hypertrophy of the follicle, and secondly, most interesting of all. the ripening follicle burrows from the depths of the cortex towards the surface of the ovary and in some way discharges the contained ovum into the peritoneal cavity. The changes in the follicle which are seen in the process of ripening will now be dealt with.
The primordial follicle consists of an ovum surrounded by a single layer of ﬂattened cells, and all these cells are derived from the germinal epithelium of the embryo. The peripheral cells later become differentiated to form the granulosa layer of a Graafian follicle. Until ripening begins there is a sharp line of demarcation between this peripheral layer of cells and the stroma cells of the ovarian cortex, but in the process of ripening two further layers become developed to surround the follicle and its granulosa layer, an outer, the theca externa, and an inner the theca intema.
Both these layers are derived from the stroma cells of the cortex. It has been suggested in the past ‘that the theca layers ar-e developed from the granulosa layer and Waldeyer held that these theca cells arose either from leucocytes or from fibroblasts. In the human ovary it is easy to trace their origin from the stroma cells, for in the earliest stage of follicle ripening the stroma cells which surround the primordial follicle become -swollen, their nuclei ovoid in shape and staining feebly ; and if a series of ripening follicles of various ages be examined it is simple to follow the development of these swollen cells into the theca interna and theca externa cells of the follicle. The second feature to be observed in the early stages of follicle ripening is the formation of new capillaries among these swollen stroma cells. It is clear that the early changes of follicle ripening are displayed symmetrically around the ovum_and it is, therefore, reasonable to conclude that they are determined by a stimulus emanating from the ovum itself.
The granulosa cells divide and subdivide and fairly early the liquor folliculi appears, usually, as pointed out originally by Nagel and more recently by Strassmann,2 in that part of the granulosa layer which is directed towards the ovarian cortex. Because of the eccentric position of the antrum folliculi and because this space does not come directly in contact with the ovum, the discus proligerus is. differentiated and because the antrum is produced towards the ovarian cortex the discus and ovum are originally directed towards the medulla of the ovary.
The origin of the liquor folliculi is an oft debated subject. One View holds that. it is produced through the degeneration of granulosa cells, the other, recently supported by Arthur Thompson3 and Strassmann, assumes it to be secreted by these cells. There is no doubt that this latter view is correct. VVith Mallory’s stain it is quite easy to make out that the liquor coagulum is found amidst the cells of the granulosa layer, and that here it is continuous with delicate processes which are thrown out by these cells and it is not uncommon to see vacuoles of secretion in the granulosa cells themselves. While it is easy to understand how the liquor folliculi is produced it is not easy to understand how the granulosa cells and the ovum receive their nutrition. Capillaries are rapidly and plentifully produced in the theca interna layer during the process of ripening, but at this stage of development of the follicle they do not encroach upon the granulosa layer, being limited by the basement membrane of this layer——the so—called membrana limitans externa. In the stage of ripening of the follicle the granulosa layer is quite non—vascular. This view differs from the opinion of Arthur Thompson,3 but I have examined carefully for capillaries in the granulosalayer and have failed to find them, It is possible that Arthur Thompson’s mat-erial was too pathological to be considered reliable. Although the question of vascularization of the granulosa layer is seemingly of no great importance it offers an explanation of some of the peculiarities of the type of ovarian hzematorna which will be described later.
Fairly early in the process of ripening the bodies of Call and Exner make their appearance. (fig. 1.) These consist of small spherical spaces in the granulosa layer each surrounded by a regular layer of radially arranged granulosa cells. These bodies are fairly obvious but it is unknown what their significance may be. Their development has been studied very closely and the views of Honoré have been confirmed. The earliest evidence of their development is the presence of a spherical globule of clear translucent material, rather yellowish in colour, lying among the granulosa cells. Around this globule granulosa cells become arranged in a regular manner to produce a covering layer one cell thick. At a later stage, although the peripheral arrangement of granulosa cells remains, the core becomes reticulated and resembles very closely the reticulum found in the antrum folliculi. No evidence has been found to support the view of Arthur Thompson that the central core of the bodies of Call and Exner is produced by a disintegration of granulosa cells. It has been impossible to trace the origin of the central globule, but it is quite certain that this precedes the production of radially arranged granulosa cells. Similar globules are not uncommonly found in the antrum folliculi. The bodies of Call and Exner persist in atretic follicles for some considerable time. In recently ruptured follicles they are soon compressed and obliterated by the rapidly growing granulosa cells.
The changes in the theca interna layer during ripening has been described elsewhere. There are two well marked changes, first the production of new capillaries among the theca interna cells and secondly the hypertrophy of the theca interna cells so that at the end of the period of follicle ripening, and also immediately after ovulation, they surpass the granulosa cells in size.
The Approach Or The Follicle To The Surface Or The Ovary
Of all the remarkable phenomena which take place in the human ovary none can surpass in beauty, or call for more wonder, than the mechanism whereby the ripening follicle approaches the surface of the ovary. This mechanism was originally and admirably described by Strassmanfi from Aschoff’s laboratory. It is clear that before ovulation‘ can occur the follicle must burrow through the cortex until it reaches the surface and that the ovum must be situated in such a position that it can be easily discharged into the peritoneal cavity. Strassmann showed that while in the early stages of follicle ripening the ovum is attached by the discus oroligerus to that part of the follicle which is directed towards the ovarian medulla—it will be remembered that the liquor folliculi first appears amidst the granulosa cells in a spot on the cortical side of the ovum—as ripening continues the cumulus rotates so that immediately prior to ovulation the discus is directed towards the surface of the ovary. Also in the process of ripening the development of the cells of the theca interna layer is continuously best marked in that part of the layer which lies towards the peritoneal cavity and this leads to the production of a wedge of theca interna cells in this situation. (fig. 2 and 5.) As these cells are actively growing not only do they burrow through the cortex but they lead to an area of diminished resistence. In this way the growing follicle develops in the direction of the surface of the ovary and consequently gradually approaches the peritoneal cavity. lt is not proposed to enter fully into the substance of Strassmann’s paper—which is of the first order, but a few additional remarks may be made.
It must be emphasized that the Strassmann phenomenon is essentially a property of ripening follicles, although traces of the cone of theca interna cells can still be seen in follicles in early stages of atresia. As regards the propagation of the follicle to the surface of the ovary it is admitted that the production of the advancing cone of theca interna cells is the fundamental cause but it is not the only factor. In the early stages of ripening the advancing cone is free of capillaries, and there is no change. in the adjacent stroma cells of the cortex. But at a later stage of ripening changes occur both in the theca externa layer and in these stroma cells. The cells of the theca externa layer immediately in front of the advancing cone hypertrophy and become irregular in outline and their protoplasm becomes vacuolated. These changes are accompanied by the production of large spaces between the theca externa cells and a particularly well marked space is seen between the two theca layers. Corresponding changes occur in the stroma cells in this situation and all these changes are factors which reduce the resistance to the development of the ripening follicle in the direction of the peritoneal cavity. It is not uncommon to see a large space produced at the very apex of the proliferating cone of theca interna cells and in some cases at this stage, because of the spaces produced, the surface of the ovary becomes depressed at the spot which is later to become the stigma. Similar changes can sometimes be observed in early atretic forms of the follicle. (fig. 3.)
Now with respect to the rotation of the cumulus. It is a fact which is easily proved by a comparative study of a series of ripening follicles that the cumulus which is originally directed towards the medulla gradually rotates until just before ovulation it lies against the spot which is to become the stigma. (fig. 3.) This arrangement will allow the ovum to be easily discharged into the peritoneal cavity. The mechanism of this rotation can be appreciated by studying a ripening follicle but it is extremely difficult to describe. It depends upon two main factors, the first is that the wl1ole follicle is surrounded by cortical stroma cells and as these are packed tightly together they constitute a rigid capsule; the second is the consistence of the theca interna layer. This layer consists of actively growing cells among which numerous young capillaries have developed and these properties give it a labile character. On the other hand the part of the follicle within the rnembrana limitans externa is relatively rigid. (fig. 2.) It therefore follows that that part of the follicle which lies within the membrana limitans externa is capable of a rotatory movement in the medium of the theca interna layer. These points are quite clear if a ripening follicle is examined, but it is not clear what stimulus effects this rotation. The following suggestions, which are not altogether satisfactory, are put forward. In the early stages of ripening, although theca interna cells develop most plentifully in the advancing cone, the theca interna layer is thickest at the opposite pole and this thickness of the theca interna layer is due to the number of capillaries found at this situation. But the layer here is not uniformly thick, it varies in different situations and this results in the production of kinks in the granulosa layer. (fig. 2.) These kinks will therefore lead to a rotatory force being brought to bear on the part of the follicle within the membrana limitans externa. This rotatory force will result in this part of the follicle rotating until its heaviest part, namely, the discus, comes to lie in the region of least resistance, namely, the proliferating advancing cone of theca interna cells.
The Histological Features or Rupture of the Follicle
Immediately prior to rupture the follicle is near the surface of the ovary with the cumulus directed towards the peritoneal cavity. The theca interna layer is proliferated in this direction and is now becoming filled with dilated capillaries; the theca externa cells are swollen, widely separated from each other, and perhaps there is a depression from the surface of the ovary at the spot which is to become the stigma. The follicle approaches the surface in this way until no stroma cells intervene between its cone of theca interna cells and the surface of the ovary. At this stage a plug of coagulated plasma appears in the most advanced part of the theca interna layer. (figs. 4 and 5.) This plug contains a few leucocytes and also for some peculiar reason a relatively large number of eosinophile cells. The resistance to the pressure within the growing follicle is now necessarily very small and the liquor bursts through the plasma plug, pushing the ovum with its corona radiata into the peritoneal cavity. Several sp-ecimens which show the state of affairs immediately after ovulation have now been obtained. In normal specimens there is no blood in the cavity of the follicle. This is now easily explained by the observation that no capillaries are found in the granulosa layer prior to ovulation. The capillaries of the theca interna layer are separated from the granulosa cells by the membrana limitans externa. As a result of the sudden release in pressure some distortion in the outline of the granulosa layer results, but this distortion is not responsible for the convoluted form of the corpus luteum. This is produced at a later stage by the enormous hypertrophy of the granulosa cells and by the formation of capillary tufts in the theca externa layer.
The stigma is now immediately closed by the plasma plug described above, and it seems tolerably certain that only for a very short time is there a communication between the cavity of the follicle and the peritoneal cavity. The second characteristic appearance in the situation of the stigma is the eversion of the layers of the follicle. This eversion is clearly produced by the sudden release in pressure within the follicle and the sudden diminution in its dimensions. Consequently, immediately after -ovulation two everted lips of granulosa cells matted together by the plasma plug represent the histological appearances of the stigma. It is believed that this represents the normal state of affairs but there are undoubtedly modifications which will be indicated below.
The temporary closure of the stigma is made permanent by methods now to be described. The following is seen quite frequently. The everted lips of the granulosa layer which are glued together by the plasma plug, subsequently become approximated through the hypertrophy of the granulosa cells in the proliferative phase of the corpus luteum. The plasma plug disappears, the two lutein layers become adherent, and in this way the stigma is permanently closed. In this method of closure, because of the eversion of the granulosa layer, granulosa lutein cells may be found spread over the surface of the ovary immediately around the stigma. (fig. 6.) This method of closure is seen best in cases in which the corpus Iuteum is well developed and the granulosa lutein cells are large.
The second method of permanent closure depends upon the growing over and the obliteration of the plasma plug by connective tissue cells derived from the ovarian cortex. It is apparently determined by two factors, first, a large stigma, and secondly, poor development of granulosa lutein cells. In these cases eversion of the granulosa layer at the stigma is not well marked, so that a glueing together of the opposing lutein cells does not occur when luteinization of the granulosa layer takes place. Connective tissue cells from the adjacent ovarian cortex gradually grow over and cover the stigma, but the site of the stigma can easily be recognized, for not only is it usual for this connective tissue layer to be depressed into the corpus luteum at this spot,_ but the connective tissue layer is thin and the Stroma cells are not packed closely together as they are in the adjacent parts of the cortex. Again, at the site of the stigma although granulosa lutein and paralutein cells have become continuous with those of the opposite side, both cell layers are ill developed at this spot, particularly the granulosa lutein cells. At the site of the stigma after permanent closure therefore, the wall of the corpus luteum is thin and represented mainly my paralutein cells.
In the third method there is no closure in the true sense of the term. In these cases. the stigma remains widely patent—in one case it was approximately of the same width as the corpus luteum itself and is not covered by connective tissue cells or by lutein cells. Nevertheless the cavity of the corpus luteum does not communicate with the peritoneal cavity for in these cases the plasma plug remains as a well—defined strip of fibrin which passes from one edge of the stigma to the other. The etiology of this latter class of case. is very simple. It depends uponthe occurrence of a large interstitial haemorrhage in the theca interna layer of the follicle during the process of ripening; the haemorrhage being in that part of the follicle immediately opposite the stigma. This heemorrhage, limited by the membrana limitans externa, pushes the adjacent grantilosa cells inwards towards the stigma so that after ovulation the part of the follicle diametrically opposite the stigma may be pushed through the stigma itself. In these cases the stigma remains Widely patent.
It is not out of place to emphasize here once more that haemorrhage does not take place into the cavity of the follicle during and after ovulation. Perhaps in some grossly hyperaemic cases a few red cells get into the cavity, but it is doubtful if large haemorrhages ever occur, for the reason that the granulosa layer does not contain capillaries at this stage and is separated from the engorged capillaries of the‘ theca interna layer by the membrana limitans externa.
It is of some interest to note that the three methods of closure of the stigma can be made out if corpora albicantia are examined. But for the replacement of the lutein layer by hyalin tissue parallel pictures are seen. But it should be remembered that corpora albicantia tend to become displaced inwards to the medulla of the ovary, and in the case of very old corpora albicantia it is impossible to make out any trace of a connexion between the corpus albicans and the surface of the ovary. Most text-books state that the grooves and furrows on the surface of senile ovaries are produced by the scars of old ruptured follicles. This is quite wrong. The grooves and furrows are produced after the active child—bearing period since, as there is no call for a large blood supply to the ovary, the vessels of the medulla become atrophied and the reduction in the bulk of these vessels results in the more rigid cortex becoming convoluted as it collapses over the atrophied medulla. This explanation is at once obvious if senile ovaries are examined histologically.
A resume has been given above of the normal processes of follicle ripening and of ovulation, partly because these processes are not widely known and partly because they form a physiological basis upon which certain pathological conditions of the ovary can be explained. The most important of these pathological conditions is a type of haematoma which occurs in relation to ripening follicles. The subject of ovarian hzematomata is very popular and its literature very extensive. But until recently deplorable errors were made, the majority due to ignorance of normal ovarian histology and physiology. It is not proposed to give an account of all forms of ovarian haematomata ; it is believed that by limiting oneself to a description of this one type its importance, its frequency and its simplicity will be emphasized and perhaps something will be done to eliminate the present day confusion.
Far and away the commonest form of ovarian haamatoma is the type due to haemorrhage into the theca interna layer of a ripening follicle. I disagree entirely with Novak’s5 statement that the commonest form is that seen with atretic follicles and I am convincedthat the stromal haematoma of Pfannenstiel is extremely rare. Further, I believe that a large number of so-called stromal haematomata belong to the type now being described but that owing to incomplete histological examinations this association has been missed. At‘ the present time there is no terminology for the type of haematoma now to be described, so it is suggested that the term follicular haematoma be employed. The term theca lutein haematoma cannot be used, since the theca interna cells have not taken on lutein characters.
It has been emphasized elsewhere1 that ovarian hyperaemia is frequently found in laboratory specimens of human ovaries and that this is related to the fact that the bulk of such specimens are obtained from cases of adnexal inﬂammation and uterine fibroids. In inﬂammatory conditions the hyperaemia is almost certainly due to the inﬂammatory reactions within the ovary. In the case of uterine fibroids the cause of the hyperaemia is not known with certainty. It is worth mentioning that ovarian hyperaemia is commonly met with in post-mortem material.
It is clear that if an ovary is hyperzemic, and ovarian hyperzemia may attain a remarkable degree, the capillaries of the theca interna layer of a ripening follicle will become engorged with blood. It is a typical finding in such ovaries that ripening follicles stand out distinctly by the gross congestion of the theca interna layers of the follicle. Further, such follicles can easily be seen with the naked eye and are responsible for the majority of haemorrhages seen in the ovaries of such cases. But in all cases the hyperaemia is limited to the theca interna layer and, because the granulosa layer is not vascularized, there is no blood in the cavity. Since the capillaries in the proliferating theca interna layer are young and delicate it follows that if the primary ovarian hyperaemia is extreme, the wall of the capillaries may be unable to resist the capillary pressure and then an interstitial haemorrhage will occur in the theca interna layer. The resulting condition is a follicular haematoma. (fig. 7.) Its anatomical features are as follows :- the haemorrhage is bounded internally by the membrana limitans externa of the follicle and does not invade either the granulosa layer or the cavity. Externally it is surrounded by the dense stromal tissues of the cortex and in no case has a large diffuse stromal haematoma been seen; it is always localized around the follicle. There is obviously a close parallel between the etiology of this form of hzematoma and the etiology of corpus luteum hasmatorna. In both cases there is a primary ovarian hyperaemia, and in both cases this leads to the rupture of the walls of delicate newly formed capillaries. In the case of the follicular haematoma these are the capillaries of the theca interna layer of a ripening follicle; in the case of corpus luteum hzematoma they are the capillaries of the granulosa lutein lay-er when this layer is becoming vascularized.
Follicular haematoma are often up to three-quarters of an inch in diameter and in such cases the haemorrhage in the theca interna layer is so extreme as almost completely to obliterate the cavity of the follicle, so that, in places, opposite surfaces of the granulosa layer come into contact. And yet even with extreme haemorrhage both granulosa layer and cavity are free of blood. The interstitial haemorrhage may lead to the formation of large masses of coagulated plasma and this finding is not uncommon.
In all cases theca interna cells can be identified among the extravasated blood cells, and in most cases a well-defined layer of theca interna cells is present immediately external to the granulosa layer. Such follicular haematomata do not apparently influence the general features of the process of ovulation, but it is not uncommon in such follicles to see a little extravasated blood amidst the plasma plug at the stigma, though severe haemorrhage into the cavity does not occur.
It has already been pointed out that the follicular haematoma is the commonest form of ovarian haematoma and the etiology described above is simple and rigorously based upon physiological processes.
There is no evidence to suppose that a hzematoma of an atretic follicle ever occurs. It is true that atretic follicles with hzemorrhagic theca layers are seen, but they represent the late stages of follicular haematomata. In very old forms the blood is absorbed to a great extent, but while the normal atretic processes continue pigmented connective tissue cells are found around the hyaline lamina, and such atretic bodies with pigmented cells in the near vicinity represent the last stage of follicular haematomata.
There is no reason to believe that such haematomata have any clinical importance. The above communication has been given in the hope that it will help to clear up the existing confusion about ovarian haematomata.
- The features of follicle ripening have been, described and the mechanism of the approach of the ripening follicle to the surface of the ovary explained.
- The histological changes at the stigma immediately before and after ovulation have been recorded.
- An account has been given of the methods of temporary and permanent closure of the stigma.
- A form of ovarian haematoma related to the alterations in the follicle during ripening has been described.
1. Shaw, W. Iourn. Obstet. and Gynarol. Brit. Emit, 1926, xxxiii, 183.
2. Strassmann, P. Arch. f. G_vm'ikol., 1923, cxix, 168.
3. Thompson, Arthur. Ioum. Anat., 1920, liv, 1.
4. Shaw, W. Ioimi. Obstet. and Gynrrcol. Brit. Emp., 1925, xxxii, 679.
5. Novak, J’. '1‘. Bull. folms Hofakins Hosp., Nov. 1917, xxviii, 3,49.
Fig. 1. The discus proligerus and ovum of 21 young Gmafiaii follicle are shown. In the lower part of the photograph a row of the bodies of Call and Exner is present. The well defined line of demarcation between the granulosa and theca interna layers is seen. Theca interna cells are not numerous in this part of the follicle.
Fig. 2. A ripening follicle approaching the surface of the ovary. The advancing cone of proliferating theca interna cells can be seen: the cells of this layer are here packed closely together. The ovum and discus are rotating to lie eventually immediately beneath the surface of the ovary. The vascularity of the theca interna layer on the medulla side of the follicle is seen and the distortion of the follicle can be made out.
Fig. 3. A follicle in the early stage of atresia. The depression on the surface of the ovary is present. In this case atresia occurred when the follicle was on the verge of rupture. The cumulus can be seen near the surface of the ovary. The cortical stronia intervening between the stlrface and the follicle is oedematous.
Fig. 4. This section was taken immediately to one side of the stigma of a recently ruptured follicle. To the right is the cavity of the follicle. There is a large hseinorrhage into the theca interna layer. The advancing cone of theca interna cells can be seen and the plasma plug is well shown.
Fig. 5. The same section under a higher magnification. To the left lies the surface of the ovary. The plasma plug, its contained leucocytcs and the advancing cone of them interna cells are well brought out. In this case there is hacinorrliage into the theca interna layer.
Fig. 6. The stigma of a corpus luteum. Below and to the right lies the cavity of the corpus luteum, above is seen the surface of the ovary. In this case the everted lips of the ruptured follicle, through the proliferation of the grannlosa cells, have become glued together and no communication between the peritoneal cavity and the cavity of the corpus luteum now exists. Paralutein cells can be seen to the left. Granulosa and paralutein cells can be seen on the surface of the ovary surrounding the stigma.
Fig. 7. A follicular haematoma. Above and to the left lies the cavity of the follicle with a thin granulosa layer. The rest of the photograph shows the theca interna layer infiltrated with blood.
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Shaw W. Ovulation in the human ovary - Its mechanism and anomalies. J Obstet. and Gynaecol. (1927) 34(3):
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