Paper - The occurrence of polyovular graafian follicles (1924)

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Kennedy WP. The occurrence of polyovular graafian follicles. (1924) J Anat. 58: 328-34. PMID 17104025

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This 1924 paper by Kennedy describes the occurrence of polyovular graafian follicles in the ovary.

Modern Notes: Graafian follicle | ovary

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The Occurrence of Polyovular Graafian Follicles

By Walter P. Kennedy. Department of Physiology, University of Edinburgh.


In the large literature on the histology of the ovary there are occasional references to the occurrence of polyovular Graafian foilicles, and in almost every case this is characterised as a rare phenomenon. In the examination of a series of ovaries for another purpose, this condition was met with in a relatively large number of specimens, which are described here.

Previously polyovular follicles have been recorded in human subjects by Schottlander (1), Nagel (2), Stoeckel (3), Rabl (4), Arnold 6); in bats by van Beneden (6); in cats by Rabl (4) and Schrén(7); in dogs by Waldeyer(i6), Bouin (8), Wagener (9) and Smyth (10), in rabbits by Wagener(9) and Honore(1); in Dasyurus by O’Donoghue (12); in pigs by Corner (13), and Schmaltz (14); and in guinea pigs by Loeb (5).

Unfortunately complete serial sections were not available in any of my cases, and the notes which follow refer only to one slide in each case.

Dog 74 was an animal of about eleven months. The ovary contained several large follicles almost ripe, and many of middle size, but relatively few primordial follicles. In places the latter were crowded together to the point of slight deformation but none were polyovular. Of the middle sized and large ones, eight were counted with two ova, two with three, one with four and one. with five ova. It is possible that serial sections would have revealed more. Fig. 1 shows the follicle containing five ova, and is particularly noteworthy in that one of the ova is separated from the others by a membrana propria, in the corner of which a few connective tissue cells may be seen. The ovary was otherwise normal except that the connective tissue was not conspicuous,

Dog S. This ovary contained two large corpora lutea, several half ripe follicles, and very few primordial follicles only one of which was biovular; six of the larger ones, however, were biovular and three triovular. One of the latter is reproduced in Fig. 2. At one side of the follicle is an old convoluted corpus luteum sear. The theca is not so well marked as is usual in dog’s ovaries. One middle-sized follicle in another part of the section lies beside a large follicle, separated from it only by the membrana propria, and causing it to bulge inwards to a slight extent. This will be referred to later. This ovary contains more connective tissue than the preceding but still less than is normal.

Cat Th. This cat had been thyrodectomised fourteen days before it was killed. There were six large follicles one of which contained two ova, at opposite poles, and a large number of primordial follicles, of which at least 15 per cent. were double. Their appearance was similar to that in Figs. 4 and 5.

Fig. 1. Polyovular follicle of Dog 74, x 50. The theca interna (th.) is well marked and one ovum is separated from the others by a membrana propria (m.p.).

Fig. 2. Triovular follicle of Dog 5, x 50. A convoluted corpus luteum scar (s.) lies at one side and several mitotic figures (mit.) can be seen in the membrana granulosa (m.g.). Notice the degenerating ovum (d.).

Cat nn. There were a large number of follicles of all stages present in the ovary and one fairly old corpus luteum with a flattened appearance; the stroma was highly fibrotic but the appearance was otherwise normal. Four large follicles were biovular, three triovular and one (Fig. 3) contained five ova, and was peculiarly flattened on one side. Many of the primordial follicles were biovular, having apparently been pressed, or grown into each other. None showed any signs of mitosis (Fig. 4).

Rabbit A. The section showed only a few middle sized follicles, but many primordial ones, In several places just below the germinal epithelium two primordial follicles had grown together so that the ova were immediately contiguous. No signs of division were observed in any of the cases (Fig. 5).

Rabbit 19. This animal had received some injections of corpus luteum substance. The ovary contained a large number of follicles, in all stages up to that of almost full ripeness, and no corpora lutea, Four of the follicles were biovular. The membrana granulosa of most of the larger follicles shows an interesting condition; some of the cells are arranged so that circular spaces are left, and these appear to be filled with liquor folliculi. These can be seen in Fig. 6 (c.s.) and to a less degree in Fig. 7, and are the “bodies” of Call and Exner.

One of the biovular follicles (Fig. 6) contained one ovum apparently normal and another markedly deformed. Under a higher power the cytoplasm of the former was seen to be granular with a few indistinct vacuoles in the centre, while the latter was very vacuolated. Another biovular follicle is shown in Fig. 7. Mitotic figures can be seen in the membrana granulosa cells,

Rabbit 0.5. The ovary contained very many follicles, mostly small, but was otherwise normal. The animal was about six months old. One large biovular follicle was found (Fig. 8).

Rabbit nn. The connective tissue of the ovary was not conspicuous, and a triovular follicle was observed wedged between two large follicles. The ova were large with well marked zonae pellucidae but the cytoplasm was degenerated.

Guinea-pig nn. A large corpus luteum occupied the main bulk of the ovary. There was one large follicle, and it contained two ova of unequal size, at opposite poles. There were only a few primordial follicles.

Fowl nn. In this case one follicle contained two closely apposed ova. The section was in other respects normal.

Several suggestions have been put forward regarding the mode of origin of this polyovular condition. Stoeckel (3) suggested that they arose from the division of a single cell body with two or more nuclei formed by amitotic division. The evidence is not strong and this suggestion has not found favour with later writers. Waldeyer(1é) was of the opinion that mitotic division of the original oocyte was the cause of polyovulation. Schottlander() held that they arise either from the division of the primordial ovum, or the inclusion of two separate primordial follicles, and that the latter is the more probable. In this he is supported by P. and M. Bouin (8), Honore (1) and O’Donoghue (2). Thelast named author points out that if a large number of ova are present within the follicle, it is unlikely that there would be no indication of division stages in the remaining follicles, and moreover, the fact that the ova are frequently in different stages of development, militates against the theory of division. Arnold’s interesting case of a woman whose ovaries showed 88 large polyovular follicles, containing up to thirteen ova, leads him to the conclusion that theories of division are not applicable to his material, but the probability is that the polyovulation is due to the development of a common follicular epithelium about two or more oocytes (5). In the present cases this seems to be the explanation in the majority, at least, though it is not quite clear whether it is due to a break down of connective tissue follicular cells or to the close contiguity of the oocytes from the earliest stages. Loeb (15) believes that the latter accounts for the origin of some polyovular follicles, but that the majority of cases are due to the intrusion of very small follicles, especially primordial follicles, into large ones. This also appears to be the explanation in some of those here, for in several cases, e.g. in Dog S, I have observed a small follicle pushed, as it were, through the theca of a larger one, and only separated from it by the membrana propria; indeed, in Fig. 1 one of the ova within the follicle is separated from the remainder by a membrana propria, to which some connective tissue cells still adhere. In no case was any evidence of mitotic division found. Loeb observed the polyovulation in the hypotypical ovary of a thyroidectomised guinea-pig and suggests that both modes of origin are due to the same cause, namely, relative inactivity of the connective tissue. Unfortunately only two case histories were available to me, viz. Cat Th and Rabbit 19, and both had been subjected to conditions calculated to bring about an hypotypical condition of the ovaries. However, several of the other specimens are somewhat hypotypical, and certainly indicate that Loeb’s explanation has a strong foundation.

Fig 3. Polyovular follicle of Cat nn, x 50. The dense nature of the connective tissue can be well seen.

Fig. 5. Biovular primordial follicle of Rabbit A, x 180. 332 W. P. Kennedy

Arnold (5) suggests that the smaller of the oocytes in a follicle containing several, might be arrested in development and probably degenerate so that all might disappear save one; or else that all might undergo atresia and never reach the stage of extrusion of the ovum. Schmaltz(14) is also of this opinion.

Several of the figures show a degenerative appearance in one or more of the ova, particularly Figs. 2 and 8, which is very probably brought about by the increased competition for nourishment.

Corner (13) suggests that a few cases of migration of the ovum may be accounted for by polyovular follicles; but the liquor folliculi does not appear to be formed in any quantity in very many of these follicles, although it is amply present in a few, and this would lessen the chances of the ovum entering the tube, according to Broman (17).

Smyth (10) reports a case of two pups from a litter of fourteen, which had several polyovular follicles in their ovaries, one follicle containing seven ova/

Fig. 6. Biovular follicle of Rabbit 19, x50. One ovum (d.) is markedly deformed in shape and circular spaces (c.s.) are seen in the granulosa. The theca interna is very well marked.

Fig. 7. Biovular follicle of Rabbit 19, x 50.

Fig. 8 Biovular follicle of Rabbit 0.5, x 50.

Another of the pups had a litter of nine at the first birth. He considers this interesting as pointing a possible correlation between polyovulation and high fertility, but this appears to be not quite justified.


Polyovular follicles are not of extremely rare occurrence and may be associated with a hypotypical ovarian condition. The mode of origin is probably partly due to primordial follicles becoming enclosed within the same theca, and partly to the intrusion of a small follicle into a large one.

The expenses of this research have been defrayed by the Earl of Moray Fund of the University of Edinburgh.


(1) ScnorrLAnpEeR. Arch. f. mikr. Anat., 1893.

(2) Naagz. Ibid. 1898.

(3) SrozcKkeL. Ibid. 1899. (4) Rasi. Ibid. 1899.

(5) ArNnotp. Anat. Rec. 1912.

(6) Van BeneDEN. Arch. d. Biol. 1880.

(7) Scuron. Zeit. f. wiss. Zool. 1863.

(8) P. and M. Bourn. Compt. Rend. Soc. Biol. 1900.

(9) Wacrner. Arch. f. Anat. u. Physiol. 1879.

(10) Smyrx. Biol. Bull. 1908.

(11) Honorsz. Arch. d. Biol. 1900. “

(12) O’Donoauus. Anat. Anz. 1912.

(13) Corner. Carnegie Inst. Pub. No. 222, 1915.

(14) Scumatrz. Quoted from Corner.

(15) Lors. Biol. Bull. 1917.

(16) WaLpEYER. Hierstock und Hi, Leipzig, 1870.

(17) Broman. Uber Geschlechiliche Sterilitat, Wiesbaden, 1912.

(18) Wetcu. ‘The Number of Oya in a Graafian Follicle,’ Bull. Lying-in Hosp. N.Y. (not accessible).

Cite this page: Hill, M.A. (2021, April 12) Embryology Paper - The occurrence of polyovular graafian follicles (1924). Retrieved from

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