Paper - Adult human ovaries with follicles containing several oocytes (1912)

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Arnold L. Adult human ovaries with follicles containing several oocytes. (1912) Anat. Rec. 6(11): 423-438.

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This historic 1910 paper by Arnold describes adult human ovaries with follicles containing several oocytes.

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Adult Human Ovaries with Follicles containing Several Oocytes

Lloyd Arnold

From the Department of Anatomy, The Tulane University of Louisiana

Four Figures


The two ovaries dealt with below were obtained at autopsy for histological purposes in this laboratory in the fall of 1909 from a negress eighteen years old. Macroscopically they appeared perfectly normal. There was no history taken of the case. When the sections were given out to the class it was found that many follicles contained more than one oocyte. It was suggested by Professor Hardesty that it might be of interest to describe the conditions found and he kindly assigned the material and the problem to me.

The ovaries were fixed in Zenker's fluid, cut transversely in celloidin at 20 micra thick, mounted serially and stained with haematoxylin and congo red. The accompanying figures were made with the aid of the camera lucida. The epithelial lining of the Fallopian tubes showed satisfactory fixation, the cell boundaries and cilia being very well defined in the sections. The connective tissue in the ovaries appeared in normal proportion, the distribution of the follicles appeared normal, and the follicular epithelium was well fixed.

Follicles containing more than one oocyte were found to be remarkably abundant. The greater number of these were in the earlier or smaller stages, varying from a follicular epithelium of one layer of cells to stages showing the beginning of the corona radiata. Of the larger folhcles only, beginning with those far enough advanced to show the first appearance of liquor foHiculi, one of the ovaries showed forty-five such follicles containing more than one oocyte. The figures below represent an accurate counting of the oocytes in each of all the follicles that were large enough to show a liquor folliculi developed: The first ovary studied gave:

17 follicles containing 2 oocytes

6 follicles containing 3 oocytes 12 follicles containing 4 oocytes

7 follicles containing 5 oocytes 2 follicles containing 7 oocytes

1 follicle containing 11 oocj'^tes

In the second ovary of the pair there were counted:

18 follicles containing 2 oocytes

4 follicles containing 3 oocytes

8 follicles containing 4 oocytes

5 follicles containing 5 oocytes

2 follicles containing 6 oocytes 2 follicles containing 8 oocytes

1 follicle containing 9 oocytes

2 follicles containing 10 oocytes 1 follicle containing 13 oocytes

Thus, in the two ovaries of the individual there was found a total of eighty-eight of the larger follicles containing more than one oocyte. The counting of the oocytes was confined to those sections of them in the series which contained the 'germinal spot' or nucleolus.

All of the sections of the first ovary studied were not available in series, a batch having been issued by the technician to the students for class work in organology before the peculiarity was observed. The section of the follicle represented in figure 1 may be taken as an example of the appearance of the polyovulation found.

The particular follicle represented in figure 1 contained eleven oocytes measuring from 110 to 180 micra in diameter, with a total average diameter of 151 micra. This follicle was not spherical in the preparations. Measured transversely in three planes from the membrana propria of the stratum granulosum on the two sides, a mean diameter of 437 micra was found for it. Its longest diameter was found to be parallel with the long axis of the ovary and therefore had to be obtained by counting the sections ill (li(> scM'ics Ihrou^li wliicli it appc-u'cd cut uiul imilti})lyinf2; l)y the known tliickix'ss of tlic sections. All of tlic (x'k'vtcs wcfc at ta('li(>(l to the stratum ^raimlosiiin by means of cumuli oopliori. H()W(>ver, fi\-e of th(MU in this case were alta(;h(>(l at. the same point by inciuis of a coiunioii pedicle, aj)i)earii).j^- through the sections collected in a grape-cluster with a common cumulus, four being attached to the fifth and this attached in the usual manner. All of the eleven oocj^tes in this follicle were normal in structure and were approximate in size to the diameters considered normal for this stage of the follicle.

Fig. 1 showing p polyovulated Graafian follicle which contained eleven oocytes. The drawing is reconstructed as far as the oocytes are concerned from a series of 12 sections each 20 micra in thickness. From the ovary of a negress of eighteen years. C, portion of a cluster of oocytes; MP, membrana propria of stratum granulosum. X 57.

The follicle represented in figure 2 is of another type of polyovulation found to 'be about equally common as that of figure 1. In this the oocytes vary markedly in size, some being three times the diameter of others. This follicle was but approximately half the size of that shown in figure 1. It contained, through the series of sections, thirteen oocytes of which five were large, averaging 150 micra in diameter, the remaining eight being smaller. Three of them were especially small, not measuring above 50 micra in diameter. All the thirteen oocytes here were attached separately to the stratum granulosum by pedicles varying but slightly in width and with cumuli oophori in about equal amount. In studying the smaller follicles, most of which were situated nearer the periphery of the ovary, it was observed that a large number of those containing more than one oocyte presented the gradation shown in figure 3. This figure was drawn to represent a smaller follicle, A, not yet developing a liquoi- folliculi and in which the oocytes were of the same size, and to represent, B,

Fig. 2 A section of a polyovulated Graafian follicle from the same individual as figure I. Shows a type in which the oocytes varj' in size. X 57.

a sinallcr f(tllicl(> with li(|ii(>i' folliculi l)('^iiiiiiii<i; to form luid wilh oii(> oocyte lai-.^cr tli;ui tlic others. These conditions were observtHl ill a hii-^e iiuiiihcr of such folUcles and polyovulated follicles of similar sizes were much more numerous than the larger sizes rt'prcstMitcd in the i)r('vious figuies.

The staining- reaction ai)})eared the same in all respects in both th(^ lai'ge and the small oocytes, the histological picture showing no indication of degeneration in any case observed beyond the variations in size.

There were quite a number of polyovulated follicles about as large as the one shown in hgure 1 which were found to contain from two to six oocytes of large size and of perfectly normal appearance. The largest follicle observed in either of the ovaries gave an average diameter of 633 micra. This contained only one oocyte whose measurements gave a diameter of 201 micra. There were two other follicles both larger than the one shown in figure 1, each of which contained but one oocyte. Thus it may be seen that the polyovulated follicles did not comprise the largest follicles.

Fig. 3 Drawing, showing sections of two smaller polyovulated Graafian follicles from same source as figures 1 and 2. .1, a smaller follicle with oocytes of equal size; B, a smaller follicle with oocytes of varying size. X 57.

Lying in the peripheral stroma of both the ovaries, mostl}" subjacent to the tunica albuginea, were the numerous primitive follicles found in all individuals. These follicles for the most part showed the usual one layer of low epithelial cells enclosing an oocyte of the smallest size (A and PF, fig. 4). Occasionally, near the periphery, several of these small oocytes appeared closely associated with each other, unevenly surrounded by an irregular line of dispersed nuclei which no doubt represented follicular epithelium in single layer.

Another interesting and seemingly unusual observation could be made in the sections of these adult human ovaries. The germinal epithelium {GE, fig. 4) appeared to be still proliferating and showed quite a number downfoldings or invaginations into

Fig. 4 Drawiiie;, showing vertical section of superficial area of ovary used foi previous figure. 6'e, Germinal epithelim; /, invagination or down cropping of germinal epithelium; V, vesicle or follicle without oocyte; PF, primar}' or resting follicles; .1, j^riniary follicle beginning further development. X 280.

the stroma below. One stage of such invagination is indicated in figure 4, /. Many stages of this could be found, including stages in which the downcroppings of the epithelium was partially and also wholly constricted from its continuation with the superficial epithelial covering, giving the appearance of short, wide tubules in the immediateh- undei'lying stroma. In no case, however, did any of the colls of these dowacroppings, or tubules, show any sign of (liflVrentiiifion into primitive oocytes. Further, follicles, or rather vesicles, could be often obstn'ved consisting of a wall of a simple layer of cells of the size of those comprising the germinal or superficial epithelium, and in every way suggesting recent formation, but, in no case did any of these follicles contain a vestige of an oocyte. They merely enclosed a cell-free space as shown in figure 4, V. A theca folliculi about these vesicles was no more definitely formed than about the ordinary primitive follicles.

If, as is generally believed, the invagination of the germinal epithelium with the differentiation of certain cells into oocytes and the formation of 'egg tubes,' 'egg nests/ and primitive follicles, terminates before or shortly after birth, or certainly before the eighteenth year, then such a downcropping and evidently resultant vesicles as seen here must represent a period in which follicles are formed but not oocytes. None of these empty vesicles were found of larger size nor were any observed 'indicating increase in size by further growth.

It is not the intent of this paper to try to explain the occurrence of the several oocytes in a single follicle. The phenomenon seems to be considered one of very rare occurrence. The first notice I have found of such in the literature is that of Waldeyer in 1870. His illustration, from the ovary of the dog, is given in Huber's revision of Bohm and Von Davidoff's Histology ('00) and is also copied by Schafer in the latest edition of Quain's Anatomy, volume 2, part 1, 1912.

Van Beneden ('80) observed in the ovary of the 'horse-shoe bat' follicles containing two or three, and in one case a follicle with four oocytes. These oocytes were of varying size and none of the follicles containing them were advanced to the stage showing liquor folliculi or follicular cavities. Schottlander ('93), working with human material, all of which was admittedly pathological, describes numerous small follicles containing two or three oocytes. Practically all in this condition possessed a follicular epithelium of but one layer of cells and these were of the primitive type. All were in ovaries of foetuses of varying ages and at term. He described some follicles, somewhat more advanced, in which there appeared a large but abnormal oocyte in the center of the follicle while certain cells of the follicular epithelium appeared enlarged as though differentiating into oocytes. These latter he called 'accessory ova.' He considered all the cases of polyovulation observed by him as degenerative conditions.

Stoeckel ('98), also working with human material, found in the ovary of a woman of twenty-nine years, several follicles containing two or more oocytes. This is the only reference I have found in the literature in which polyovulation has been observed in adult human material. Bouin ('00), reports finding in the ovary of the dog follicles containing two, and some, three, oocytes. He describes one follicle in which he estimates the presence of ten oocytes. All these, he describes as perfectly normal in appearance, the latter case being a larger follicle with perfectly normal stratum granulosum, and none of them showed any sign of pyknosis or other degenerative changes.

Honore ('00), working with ovaries of the rabbit, describes a few follicles containing more than one oocyte and one containing as many as four. These oocytes were of varying size in the follicle, and the follicles were of the smaller stages. The follicle containing four oocytes showed one in its center while the other three were much smaller and were buried among the cells of the follicular epithelium, similar to those described by Shottlander.

He describes these smaller buried oocytes as undergoing atrophy. He cites Nagel and Rabl as having observed polyovulation but does not state the animals in which they found it and I have not been able to consult their papers.

The Bouins ('00) described a follicle in the ovary of the adult bitch which contained eleven oocytes. These were very varied in size and position, the smaller being buried among the cells of the follicular epithelium as was observed by Honor^.

As to the origin or cause of such polyovulation, Bouin and Honore considered these several oocytes as having been imprisoned in the same connective tissue theca at the time of the closing off or constriction of .the egg tubes or egg nests into separate follicles.

A\';il(lrv('r thought that, in the jxtlyovulation observed 1)\' him, the additional (XK'vtes arose by mitotie division of the oocyte previously existing in the follicle, and Nagel, quoted by Honor^, seems to have supported Waldeyer in this view.

Stoeckel held that polyovulation results from the cytoplasmic division in a follicle of oocytes originally containing two or three r.uclei, and that the separate oocytes thus arising become dispersed in the follicle by the subsequent proliferation of the cells of the follicular epithelium.

Rabl, quoted by Honore, held that the follicular epithelium encloses more than one oocyte from the beginning of its formation. This may mean that from the stage commonly known as that of the 'egg nests of Pfliiger,' two or more closely associated oocytes may become surrounded by a common follicular epithelium and thus remain. He believed that polyovulated follicles are subsequently separated into monovulated follicles by the proliferation and ingrowth of the follicular epithelium, followed by the ingrowth and development of the theca folliculi. This view, however, can apply only to the younger stages of follicular development and not to the conditions found in larger follicles as observed in tliis paper. Honore himself seems unable to arrive at a definite explanation of polyovulation, but is inclined to support the views of Rabl.

In the adult human ovary here mentioned, . the tissues in all respects seemed normal. No evidences of degeneration were observed and the material was well fixed. The only peculiarities noticeable were the abundant instances of polyovulation and the evident downcropping at this age of the germinal epithelium and the formation of vesicles or follicles not containing oocytes. No evidence of cell division, nuclear or cytoplasmic, were noticed in any of the oocj^tes. Therefore it is improbable that the views advanced bj- Waldeyer, supported by Nagel, and that advanced by Stoeckel are applicable in this case. The fact that in about one-half of the polyovulated follicles studied here certain of the oocytes were much smaller than others may indicate that these smaller oocytes have been arrested in their development. Very probably such would degenerate during the further advancement of the process of ovogenesis. Possibly all would disappear except one. Or, possibly all such follicles would undergo atresia and thus never reach the stage of extrusion of the ovum.

In the series of sections of these ovaries, there may be seen in the stroma immediately underlying the tunica albuginea and among the primitive or resting follicles, series of smaller oocytes closely associated in lines of three or four, an entire line being bounded about by a single line of nuclei of follicular cells but with no follicular cells between the oocytes. Again, small clusters of oocytes appear in which certain of the oocytes seem to lack a separatel}^ distinct follicle. This condition is paitially indicated with two of the oocytes shown in figure 4, PF. It is therefore, possible that some of the polyovulated follicles of the advanced stages may result from the development of a common follicular epithelium about two or more oocytes.

Of course, nothing definite may be advanced as to whether two or more oocytes in a follicle ever proceed in their development though the stages of maturation and thence result in an expulsion of two or more ripe ova from a single follicle.

I wish to acknowledge my indebtedness to Professor Hardesty for his suggestions and guidance in the preparation of this paper.

Literature Cited

Van Beneden, Ed. 1880 Contribution a la connaissance de I'ovaire des mammiferes. L'ovaire du Vespertilo murinus et du Rhinolophus ferrumequinum. Archives de Biologie, torn. 1.

BouiN, P. ET M. 1900 A propos du follicle de graaf des mammifer6s follicles , polyovulaires. Mitoses de maturation prematurees. Compt. Rend. Soc. Biol., Paris, 13 Jan., torn 5.

ScHOTTLANDER, J. 1893 tJber den Graaf'schen FoUikel, seine Entstehung beim Menchen und seine Schieksale beim Mensch und Saugethiere. Arch, f. mikr. Anat., Bd. 41.

Stoeckel, W. 1898 Ueber Theilungvorgiinge in Primordiel-Eiern bei einer Erwachsenen. Archiv. f. mikr. Anat., Bd. 53.

Waldeyer, Eierstock und Ei. 1870 Leipzig.

Honor6, Ch. 1900 Recherches sur l'ovaire du lapin. Archives de Biol., torn. 17.

Cite this page: Hill, M.A. (2021, June 24) Embryology Paper - Adult human ovaries with follicles containing several oocytes (1912). Retrieved from

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