Paper - Internal migration of the ovum (1921)

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Corner GW. Internal migration of the ovum. (1921) Johns Hopk. Hosp. Bull. 32: 78.

Internal Migration of the Ovum

George W Corner (1889 - 1981)
George Corner (1889 - 1981)

by George W. Corner

From the f!talio)i for Experimental Evolution of the Carnegie Inst.

J-ahunitorij of The Johnt

In contemplating the passage of fertilized ova from the Graafian follicle to their resting-place in the uterus, observers have often been struck by the fact that au egg discharged from a given ovary may pass through the opposite tube, or when the uterus is bicornate, may actually find lodgement in the opposite cavity. Long tubular bicornate uteri like those of swine offer ready demonstration of migration of the ovum, for it is a very frequent observation indeed (about once in three cases) that one horn of a pregnant uterus contains more embryos, the other less, than the number of corpora lutea

titiifiiiii. Coll! SpriiHi Uurhor. Lonii Island, and the Anatomical Hopkins Uniiersitii i

The frequency of migration of the ovum in tiie human subject is not known, but may be crudely estimated by various means. Mayrhofer (1876) considered that migration must occur at least once in 10 ovulations. The present writer (Corner, 1915) found from a study of \'i8 pregnancies in swine that in this sj^ecies one or more ova migrate in at least one-third of all cases. An exact statement cannot be made in the corresponding ovary. To cite one example of hundreds available, it was found in a certain sow (Fig. 1) that the left ovary contained seven recent corpora lutea, the right ovarv' two; the left uterine cornu four fetuses and the right five. Three of the embryos in the left uterine cornu had originated, therefore, in the right ovary. Like conditions have long been known in other animals with similar uteri.

Fig. 1. — Ovaries and uterus of pregnant sow in which migiation has oreiiiied Se\en coipora lutea In left ovary, two in right ovary; four fetuses in left cornu fi\e in light cornu One fourth natural size.

In the human uterus, with its single cavity, migration of the ovum will not be detected except under peculiar conditions, hut numerous clear cases have been described. In many tubal pregnancies the corpus luteum has been found in the ovary opposite to the pregnant tube; for an especially convincing case of this type the reader is referred to one reported by Williams (1917). Migration has also been seen in cases of pregnancy in bicornate uteri, and offers at least a plausible explanation of cases such as those reported by Kelly (1906) and Winekler (1!)05), in each of which one ovary and the opposite tube were removed, but nevertheless the patients subsequently became pregnant.

because the data are obscured by non-development of one or more embryos in four-fifths of the litters.

It is obvious, as first pointed out by Kussmaul (1859), that there are two possible pathways of migration. Either the ova pass from the ovary into the abdominal cavity and thence directly into the opposite tube (external migration, fig. 2.) or they travel by way of the homolateral tube into the uterus and thence to the place of implantation in the contralateral uterine cornu or Fallopian tulie (internal migration. Fig. 3). External migration is not possible in those mammals in which the distal portion of the tube forms a closed pouch or ovarian capsule about the ovary, as in the rat (Fig. 4) and guineapig ; but no such anatomical bar exists in man, rabbit or cat, in which the tubal extremities open freely into the abdominal cavity. In these animals it is conceived that the possibility of external migration is further enhanced by the action of the ciliated lining and possibly by peristaltic movements of the Fallopian tubes, which produce currents in the films of abdoininal fluid between the pelvic organs, by which ova may be drawn into the open ostia. Experimental evidence of external migration has been given by Leopold (1880), who excised one tube and the opposite ovary in rabbits, and found the animals still capable of bearing young.

Fig. 2. — Diagram illustrating external migration of the human ovum. Four-fifths natural size.

Fig. 3. — Diagram illustrating hypothetical internal migration of the human ovum. Four-fifths natural size.

Fig. 5. — Illustrating form of the Fallopian tube of the sow, theoretically permitting migration of the ovum by either route. Two-thirds natural size.

Fig. 4. — Illustrating closed ovarian capsule of Fallopian tulje in the rat, which makes external migration of the ovum impossible. X 7.

Fig 6 — Diagiam constructed fiom the verbal description of Andrews case of supposed internal migration of the human ovum (see text).

With the rarest exceptions, all convincing human cases of migration of the ovum are capable of explanation by the external route. No conclusive evidence, clinical or experimental, has been found to show that internal migration occurs, and thus it has remained merely a hypothetical possibility. Andrews (1913-13), however, has recently reported a case (Fig. 6) which seems to fall into this class, since there was an interstitial pregnancy in tlio right side which could be excised without opening the uterine cavity, witli a normally implanted twin embiyu in the uterine cavity, in a woman whose right tube and ovary were entirely absent.

Undoubtedly, however, much of the supposed evidence for migration from clinical cases has been uncritical or incomplete, so that Burckhard (1904) did not hesitate even to deny the occurrence of fliigration by either route, except in a few human • cases in which there is a previous abnormal aiTaugement of the pelvic organs. Under this exception he admits some of the cases of tubal pregnancy in the contralateral tube, as described above. In those human and experimental cases in which previous excision of a tube is part of the mise-enscene, ' he feels that the possibility of subsequently recurring patency of the stump has not been sufficiently considered ; and in the study of animals with bicornate uteri and large litters, he believes errors have arisen in consequence of the failure of some of the corpora lutea to develop or to persist, or, on the other hand, because no allowance was made for the possible persistence of corpora lutea from previous ovulations. Although these objections are not all tenable, they riiust at least be considered in future attempts to demonstrate one or the other kind of migration of the ovum.

With respect to the pig, the present writer has direct information as to the possible causes of error suggested by Burckhard. As before pointed out (Corner 1915), there is no likelihood of confusing corpora lutea of different ovulations, owing to their rapid retrogression; while failure of corpora lutea to develop or to persist during pregnancy has never been observed in a rather large experience. Polyovular follicles undoubtedly occur and may perhaps even attain full development and discharge of their ova, but they are rare, and no experienced student of the ovary could belie\-e them sufficiently numerous to explain away a frequency of migration amounting to one-third or more of all pregnancies. Therefore, as will be confirmed by additional evidence to be given below, in the pregnant sow the number of corpora lutea found in the ovaries probably represents with perfect accuracy the number of eggs which were discharged into the Fallopian tubes at the ovulation wliicli gave rise to the pregnancy.

The Evidexce for Intekxal Migkatiox In the writers previous brief discussion of migration of the ovum in swine, to which reference has already been made, it was assumed that the cases were of the external variety, merely because this hypothesis had been proven more likely with regard to the human cases. Kiipfer (1920) who has studied seven cases of migration in swine, makes the contrary assumption as to the route. In this guess he is correct, for the statement can now be made that after all, in the pig, external migration has not been demonstrated, biit that migration of fertilized ova by the internal route is a frequent plienomcnon of physiological significance.

The evidence wdiich not only demonstrated internal migration, but also suggests some of the factors which regulate the process, has been extracted from data gathered (for another purpose) during a detailed examination of the ovaries and uteri of 54.5 sows. The work was done during a stay at tlie Station for Experimental Evolution of the Carnegie Institution of Washington, at Cold Spring Harbor, Long Island, and the -writer is most grateful to the Director, Dr. C. B. Davenport, for the opportunities afforded. Further thanks are due to ilessrs. Joseph Stern and Company, meat packers, of New York City, for material, and tv 'S\v. Clyde E. Keeler for assistance.

Template:Corner1921b table 1

Twenty-six consecutive sows were selected, by the appearance of the ovaries, as having ovulated within the past three day? : the ova were therefore en route through the Fallopian tube-;, and were actually recovered therefrom, by a method previously described (Comer and Amsbaugh, lliK). By using great care in tlie ]irocedure, and washing nut caili tube as often as five times when necessary, it was found possible to collect from a given sow, with almost mathematical certainty, all the ova expected on the basis of the corpus luteum count. In all 26 sows examined, there was a total of 220 corpora lutea, against which 213 ova were regained from the oviducts, or 96 per cent of those expected (Table I).

Template:Corner1921b table 2

Showing Distribution of Embryos in Uterus, When Equal numbers of ova were discharged from each ovary

The reader will have noticed that not only practically all the discharged ova are readily discoverable, but also that the eggs in a single tube are always accounted for by the discharged follicles (corpora lutea) in the corresponding ovary. In these 26 consecutive cases, then, there was no case of external migration.

Next a similar table was made by counting the corpora lutea and the embryos of nearly 500 pregnant sows which were passing through the same abattoir. In these animals, in spite of the fact already mentioned, that a large early embryonic mortality obscures and lowers the apparent proportion of migration, still (as was found some years ago) about one-third of the sows show migration of one or more ova. If distributed, for the sake of comparison with the first series, into groups of 26, no such group contains less than five cases in which migration occui-s.

These two facts, that migration in general is verj- common, but external migration rare or non-existent, together prove the occurrence of internal migration of the fertilized o^nim of the sow.

We may now venture the hypothesis that the phenomenon , of internal migration has a practical utility in the pig; it is important that the individual embryos of the large litters shall each find a fair share of space in the uterine cavity. As shown by the examples in Table I, the right and left ovaries often discharge very unequal numbers of ova, which might well lead, were it not for migration, to the overcrowding of embryos in one cornu.

Template:Corner1921b table 3


Showing Distribution of Eiibryos in Uterus, When the Total

Number of Ova Discharged was Uneven, One Ovary

Migration beyond balance.

This suggestion was tested by analysis of the records of the l>reaiiant uteri, frmn tlie whole series only those cases. ll:> in

number, being chosen, in wliich all the corpora were represented by normally implanted embryos, thus avoiding the obscuring effect of early embryonic degeneration. If migration is by rule and not by chance, then in these cases we should find : (1) that when the ovaries discharge equal numbers of ova. the number of embryos in each chamber remains equal; (2) liowever unequal the output of the two ovaries, the number of embryos in the uterine comua should tend to approach equality. It will also be clear that cases which deviate from these expectations should be commonly those in which the litters are small, and further that they will be damaging to the hypothesis in proportion to the number of ova which in any one case migrate in the adverse direction.

I. In 21 cases the ovaries discharged equal numbers of eggs. By hypothesis there should have been no migration. Eesult: no migration in 17 cases, but in four cases there was migration of one ovum in each (Table II).

II. In 24 cases the total number of eggs discharged was uneven, one ovary exceeding the other by one egg. In this circumstance, by our hypothesis it is a toss-up whether or not one ovum shall migrate, as the balance cannot be perfectly restored. Eesult: no migration in 14 cases; migration of one ovum in 9 cases; migration beyond balance in one case : migration toward excess side, no case (Table III).

III. In 68 cases, the output of one ovary exceeded that of the other by two or more eggs. By hypothesis there should have been migration toward the lesser side in all cases. Eesult : in 21 cases perfect balance was obtained by migration; in 20 more, the total number of eggs being uneven, balance was restored to ±i. In 3 cases, in all of which the discrepancy between the ovaries was great, perfect balance was not quite attained in the uterus (Cases 113-115). In 9 cases migration did not stop at an even balance ; in 7 of these one ovum too many went over, in 2 cases two ova migrated beyond the balance, in no case, however, forcing more than seven embrj-os into tlie uterine chamber. In 14 cases there was no migration at all, but in all these the original imbalance was small in degree, so that the need of migration was slight. In one case there was migration of one ovum toward the excess side (Case 139, Table IV).

To sum up, the hypothetical expectation was fulfilled in 84 of 113 cases, with 29 deviations, all of which were trivial in degree; hence the supposition that the process of internal migration is tmder physiological regulation for useful ends seems to be justified.

The anatomical mechanism of internal migration is now open to conjecture and experiment, but there can be but little doubt that the embryos are shifted by the peristaltic action of the uterine musculature. Some such action must be postulated in any case to account for the regular spacing of the implanted embryos within the uterus ; and the only novelty in the present contribution is the notion that both comua act as one continuous tube, which must be readily capable of peristalsis in either direction. It may well be also that the peculiar form of the ungulate blastodermic vesicle, which reaches the length of 30 or more centimeters "before implantation, may render it espe

Template:Corner1921b table 4


Showing Distributio:^ of EireRTOs in Uterus, Whex the Octptjt

OF the Ovaries was Unequal. One of the Ovaries

daily suitable for transportation by the uterus. It will be of much interest to learn whether migration of the pig's ovum can be demonstrated before the tenth day, while it is still minute and spherical.

If the forgoing discussion has any bearing upon the clinical side of the question, it is that internal migration of the human ovum is still to be regarded as occasionally possible, more especially perhaps in cases of multiple gestation. Twin embryos were present in the case of Andrews, previously mentioned, which is up to the present the most satisfactory case among those interpreted as examples of this form of migration in the human.


Andrews, H. R. : 1912-13. A case of simultaneous intra-uterine and extra-uterine pregnancy, witli probalile " internal wandering " of the ovum. Proe. Roy, Soc. Med. London. Oljstet. and Gyn. Sect., 52-53.

Burckhard, G. : 190-1. 1st eine innere und iiussere Ueberwanderung des Eies moglieh? Ztsch. f. Geb. u. Gyn., LIV, 470-484.

Corner, G. W.: 1915. The corpus luteum of pregnancy, as it is in swine. Publication No. 222 (Contributions to Embryology, No. 5) of the Carnegie Institution of Washington.

Corner, G. W., and Amsba ugh. A. E. : 1917. Oestrus and ovulation in swine. Anat. Rec, XII, 287.

Kelly. H. A.: 1906. Operative Gynecohigy. (2d Edition) vol. 2, p. 185.

KUpfer, M.: 1920. Beitrage zur Morphologic der Weiblichen Geschlechtsorgane bei den Siiugetieren. Viertcljahrschrift der Xaturforsch. Gesellsch., in Zurich, LXV, 377-433.

Kussmaul, A.: 1859. Von dem Mangel, der Verkummerung und Verdoppelung der Gebilrmutter und der Uel^erwanderung des Eies. Wiirzburg (quoted by Williams, 1917).

Leopold, G.: 1880. Die LTeljerwanderuiig der Eier. Arcli. f. Gvn., XVI, 22-44.

Mayrhofer. C: 1876. Die gelben Kiirper und die Ueberwanderung des Eies. Wiener Med, Wclinschr.

Williams, J. Whitridge: 1917. Obstetrics, Chapter 3.

Winckler: 1905. Ein Fall von Ueberwanderung des Menschlicheu Eies. Verb, deutsch. pathol. Gesellsch., Jena, VIII, 177.

Cite this page: Hill, M.A. (2024, February 28) Embryology Paper - Internal migration of the ovum (1921). Retrieved from

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