Book - Contributions to Embryology Carnegie Institution No.56-10

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Chapter 10. Alleged Occurrence of Superfetation

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Mall FP. and Meyer AW. Studies on abortuses: a survey of pathologic ova in the Carnegie Embryological Collection. (1921) Contrib. Embryol., Carnegie Inst. Wash. Publ. 275, 12: 1-364.

In this historic 1921 pathology paper, figures and plates of abnormal embryos are not suitable for young students.

1921 Carnegie Collection - Abnormal: Preface | 1 Collection origin | 2 Care and utilization | 3 Classification | 4 Pathologic analysis | 5 Size | 6 Sex incidence | 7 Localized anomalies | 8 Hydatiform uterine | 9 Hydatiform tubal | Chapter 10 Alleged superfetation | 11 Ovarian Pregnancy | 12 Lysis and resorption | 13 Postmortem intrauterine | 14 Hofbauer cells | 15 Villi | 16 Villous nodules | 17 Syphilitic changes | 18 Aspects | Bibliography | Figures | Contribution No.56 | Contributions Series | Embryology History

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From time to time reports of alleged and apparent instances of human superfetation appear in current medical literature. Reports of similar instances in other mammals occur also, although more rarely, in the nonmedical literature. As recent instances of the former may be cited the cases reported by Logan (1917) and Gustetter (1918). Of instances of the latter may be mentioned the cases of King (1913), Sumner (1916), and Harmann (1917, 1918). The latter group of cases were found in the rat, the mouse, the cat, and the cow, respectively.


Without accepting the alleged or apparent cases in mammals with bicornuate uteri as unequivocal, it is easy to see that, aside from ectopic implantations, the conditions under which superfetation necessarily would have to occur in the human uterus may be totally different from those that may obtain in bicornuate uteri. Since the usual intermenstrual period in women is 28 days, it would also seem, as often asserted, that the older of two fetuses in a case of human superfetation certainty would occlude the uterine cavity rather effectively, and alone make fertilization of any ovum, liberated at a subsequent ovulation, difficult. It would seem to do this, entirely aside from the possible effect of the cervical mucous plug so frequently referred to in the literature.


These things are true especially in such instances as that of Gustetter, in which the time interval between the ages of two fetuses is estimated to have been as great as 65 days. Moreover, it would seem that the development of the first fetus and that of the corpus luteum in such a case as this would have inhibited the occurrence of subsequent ovulations. An obstacle to the implantation might also be found in the condition of the decidua, even if later ovulation actually occurred. Since Loeb (1912) found that in the pregnant guinea-pig the endometrium can not be stimulated to form a new decidua, it is evident that the fertilized ovum might encounter insuperable difficulties if similar conditions obtain in the human being. However, if a young blastocyst really can become implanted on the bare surface of an ovary, or on the peritoneum even, then it may well be doubted whether a new decidual reaction is essential for implantation of the ovum in the human being. Furthermore, when implantation in the Graafian follicle occurs, there is no decidual reaction, at least nothing comparable to what occurs in the uterus, although the proliferating luteal cells may possibly act vicariously to some extent. However, there are other obstacles to superfetation, such as those mentioned above and the possible occlusion of the uterine tubal orifices in consequence of hyperplasia of the uterine musculature and mucosa.


Although it is being established that ovulation and menstruation apparently are not contemporaneous phenomena, succeeding ovulations nevertheless probably are periodic and separated by a considerable interval of time from each other. Such a conclusion seems to be fully warranted, although it is, of course, well known that ovulation may occur without menstruation in normal nonpregnant women. This, however, does not establish the occurrence of ovulation during pregnancy. According to Fraenkel (1910 b ) and Miller (1910), ovulation normally precedes menstruation by about 9 days; but from a study of 100 cases in which the time of occurrence of the menstrual period and the approximate time of coitus were known, Siegel (1915) concluded that ovulation usually occurs between the seventh and fourteenth day post menstruum. Cosentino (1897) and also a few others have reported cases of ovulation during pregnancy in women, but we unfortunately know little as to the exact conditions which obtain, so that the entire matter remains as yet rather undecided.


Franco (1910), while reporting a case of spurious superfetation, gave a long list of Italian writers who were said to believe in the occurrence of superfetation. Unfortunately, this literature at present is largely inaccessible to me in the original, and such as is accessible remains unconvincing, as all of it apparently seemed to Cuzzi, who is reported by Franco as regarding superfetation only as a theoretical -possibility. Nor does there seem to be good evidence that ovulation occurs during pregnancy in other higher mammals. The only case cited is the questionable one in a cat reported by Christopher (1886) . At present it has not even been established that superfetation occurs in the rare cases of double ovarian or of combined ovarian and uterine pregnancies, although these cases would seem to furnish far more favorable conditions. Did the alleged occurrence of superfetation not involve a series of assumptions each one of which remains unproved, belief in it would seem easier. Consequently, in view of all these things, the conclusion of Gustetter that superfetation is "a frequent though often overlooked cause" of abortion in women seems rather venturesome, and anyone who critically examines Herzog's (1898) article will see that the evidence he presents really does not justify the claim that it "demonstrates fairly well that there is very little if any reasonable doubt left as to the occurrence of superfetation in the human race." Indeed, although the cases here presented would seem to offer far more conclusive evidence of the occurrence of superfetation than any presented heretofore, there is no doubt that such an interpretation of them would be a mistaken one.


The possibility of superfecundation, however, is not necessarily excluded by these considerations, for ova from the same ovulation still might be fertilized at somewhat different periods by some spermatozoa from the same or from subsequent coituses. But even while theoretically possible, it is evident that the relatively limited period of vitality of the unfertilized ovum, as contrasted with the duration of pregnancy, would make it extremely difficult, if not impossible, to recognize such cases. This would be true even if they occurred in the earlier stages of development, for normal growth differences are too great when contrasted with the greatest differences that could possibly exist under these circumstances. This would seem to be true even if we grant that the spermatozoa have a somewhat more tenacious life than ova. Mall (1918) considered evidence which seems to indicate that the life of the fertilizing power, even if not the life of the spermatozoon, is a decidedly limited one. Hence, if this be true, superfecundation is limited still further as a factor in the problem of superfetation.


In all instances in which the discrepancy in size or development between two fetuses is such as to suggest that one of them arose from an ovulation so far removed from the other as to produce unusual differences in size in the later months of prenatal development, the assumption of independent action of the ovaries, considered by King in the case of the rat, would not avoid the foregoing difficulties. Nor could the occurrence of deferred fertilization, which is 'advanced by Sumner as an explanation for the occurrence of supernumerary broods in mice, be used as an explanation in human cases, for the period of vitality of both the ovum and the spermatozoon would seem to be entirely too short to become responsible for marked development differences.


Sumner found supernumerary litters to occur in 3 per cent of 250 broods in young mice. Such litters were particularly frequent in young deer mice. The frequency of supernumerary broods would seem to vary greatly in closely allied mammals, however, for King observed only 2 cases, and these she regarded only as "seemingly" instances of superfetation, among 700 normal broods of rats. This is an incidence of 0.28, or a frequency only one-eleventh as great as that found by Sumner in mice. Sumner also stated that more than 80 per cent of the supernumerary broods survived nearly or quite nearly to maturity, and King added that all of those broods in rats were raised to maturity and that some were used for breeding purposes later.


Although both King and Sumner regarded the occurrence of superfetation with considerable reserve, neither seems to have considered the possibility of delayed parturition in one horn of the uterus as worthy of consideration in connection with supernumerary broods between which the time interval was short. Whenever this interval was relatively long as contrasted with the gestation period, such a suggestion is untenable, unless corresponding developmental differences were present. It might be helpful as well as interesting to make a careful gross and microscopic examination of the broods concerned in order to contrast the respective states of development.


Since L. Fraenkel (1910 b ) found that some rabbits copulate while pregnant, it would be of especial interest to know if supernumerary broods are particularly common in such rabbits, and whether supernumerary broods can be produced in mice should comparable conditions obtain. A particularly interesting question would seem to be raised by the occurrence of such cases as reported by Guerra (1909), in which a second implantation is said to have occurred while a dead fetus still was retained in utero. Under these circumstances the smaller, younger fetus should always be best preserved. Although ovulation, and perhaps also menstruation, could occur under such circumstances because of the occasional regeneration of the endometrium, even before abortion, one scarcely can regard such a sequence of events as established at present. However, Franco (1910) stated that there is no lack of cases in which a second pregnancy occurred under such circumstances. But that does not establish the occurrence of superfetation, for in a physiological sense death of a conceptus really terminates a pregnancy. Since at least partial regeneration of the endometrium may occur in the presence of a dead conceptus, it is conceivable that a new implantation might occur in spite of the presence of a dead conceptus. This, however, would be a case of pseudo-superfetation only, for if the term has any real significance it can only mean the superposition of a second pregnancy upon one that is still living.


Sumner quite rightly called attention to the fact that in the great majority of cases of superfetation recorded in man, one or both fetuses were macerated before born, and King concluded that "many cases that have been reported as due to superfetation unquestionably are instances of superfecundation or of blighted ova." Nevertheless, King regarded the case in a sheep reported by Arrowsmith (1834) as probably genuine, and added that "although Christopher found that ovulation might occur during pregnancy in the cat, superfetation is not known to occur in this animal." However, Jepson, in 1883, reported such a case, and Harman (1917) another. Neither report, however, would seem to bear critical scrutiny, although both are quite as trustworthy as other reports of alleged superfetation. In the case of Harman it would seem more probable that intrauterine death of one fetus with survival of the other was responsible for the misconception. It should be recalled that such instances are relatively common in the rat, guinea-pig, rabbit, ferret, marmot, pig, and some other mammals. These phenomena have been discussed by Strahl and Henneberg (1902), Henneberg (1903), L. Fraenkel (1903), Koebner (1910), Huber (1915), Mall (1915), and Meyer (1917 a ).

Figure 149.

As is evident from figure 149, in which the so-called younger superfetus, reported by Harman in a cat, is contrasted with a normal cat fetus (fig. 210, plate 8, Chap. XIII) of approximately the same length, the latter has a totally different form. The same thing is evident also, although to a lesser degree, on comparing the illustration accompanying Harman's article with one from Kunz (1916), shown in figure 150. Since the latter, the larger of two macerated apparent superfetuses, in the report of Kunz, was deformed by retention, it may have measured a little more or less probably more than 10 mm. at the time of its death. However, even were it a trifle older than the fetus in figure 210, as its form would seem to suggest, the difference is slight and may be ignored for purposes of comparison. Kunz spoke of the larger fetus, shown in figure 150, as entirely normal, which it apparently was, for the deviations from the normal form (figure 210), which the illustration so clearly shows, undoubtedly are due to post-mortem, ante-partum changes so common in human abortuses. Kunz's conclusion that all three fetuses in his case in the cat resulted from ova which were fertilized approximately at the same time heartily commends itself. Kunz further concluded that these specimens furnish no evidence for the occurrence of superfetation, in spite of the fact that two smaller macerated distorted fetuses, which were only 9 and 10 mm. long, accompanied a nearly full-term fetus.


Harman (1918) also reported a case in the cow which, however, she regarded merely as one of "probable superfetation." Unfortunately this report rests very largely on the statement of a veterinarian, who made no further examination of the specimen. Hence it would seem that we have no unequivocal evidence regarding the occurrence of superfetation, even in mammals other than man. Moreover, as far as man is concerned, the large amount of literature on the subject furnishes no cases more convincing than that of Calderini (1909). Most of them can be easily recognized, from the reports alone, as probable instances of twin pregnancy, in which one fetus died and then was retained until the birth of the other. Confusion is due largely to the fact that dead fetuses often are retained for a considerable period without showing very evident changes in form or gross structure. This seems to be due, in part at least, to retardation in the lytic processes in embryonic as compared with adult tissues, a phenomenon which has been referred to the slow post-mortem development of acidity in embryonic tissue.


Since external form is mainly relied on as a criterion by the general practitioner, it is easy to see how misinterpretation of the facts arises, and it is significant that it is only the specialist who has come to doubt that superfetation ever occurs in human kind. This assumes, however, that by superfetation is meant the partly simultaneous intrauterine development of two or more fetuses derived from ova liberated by independent ovulations separated from each other by a considerable period of time ; or, in brief, the superposition of one pregnancy upon another.


Since most reports on superfetation concern fetuses in the later months of pregnancy, it occurred to me that a representation of certain instances of twin pregnancy from the earlier months of pregnancy might be of special interest, because such specimens could more easily and rightly be taken for examples of true superfetation. In the cases under consideration, one fetus evidently died some time before the abortion of both, a circumstance that resulted in considerable differences in age and form between the two. An examination of the accompanying cases will make it clear that all the instances here reported easily could be included among the alleged instances of superfetation found in the literature without doing the least violence to that literature. More than that, the instances here reported would form fine examples among such cases.


The youngest specimen contained in the Carnegie Collection which came to my attention, and which might be regarded as one of superfetation, is No. 587, donated by Dr. F. A. Conradi of Baltimore. The cavity of the larger chorionic vesicle in the fresh specimen measured 32 by 23 by 23 mm., and that of the smaller about 6 by 6 by 9 mm. The latter was empty, but the former contained a cylindrical embryo 7 mm. long which Mall found greatly dissociated with a practically solid brain and only a remnant of the intestine. The amnion was present, and as shown in figure 31 (plate 4, Chap. IV), both vesicles formed a single mass which was covered by infiltrated decidua. That these chorionic vesicles both once contained an embryo, no embryologist will doubt. It is evident also that both were retained for some time after life and growth had ceased. The gross and histologic appearance of the entire specimen alone is sufficient proof of this. Although the smaller chorionic vesicle was incorporated in the margin of the larger, its death did not lead to its abortion or to that of the surviving twin. Yet the smaller of these twins undoubtedly died a considerable period before the larger. This is indicated also by an examination of the specimens and by the presence of decidua between the villi belonging to the respective vesicles at a point where they come in closest contact. An examination of this area shows that the ovum giving rise to the smaller conceptus was embedded independently, although undoubtedly also contemporaneously with the larger. Hence this specimen can not be rightly regarded as one of superfetation.


The next specimens of twin pregnancy which might be regarded as a case of superfetation are Nos. 788 a and b, donated to the Carnegie Collection by Dr. Anfin Egdahl. These twin chorionic vesicles, which were almost of the same size, measured 60 by 45 by 40 and 60 by 55 by 40 mm., respectively. Although of approximately the same size, the former contained a stunted embryo 17 mm. long, the latter a nodular one only 3 mm. long. The differences in size and in the character of the two embryos are so marked that they prompted Mall to make special inquiry of the donor as to whether these chorionic vesicles were really obtained from the same patient, as reported. This inquiry Dr. Egdahl was able to answer promptly and positively in the affirmative. Here we are again dealing with a case of twin pregnancy, in spite of the fact that the size of the embryos might seem to indicate that we really have a case of superfetation under consideration. But that the case is not such is shown also by the fact that the chorionic vesicles practically are of the same size. The smaller abortus with a partially inverted chorionic vesicle containing the better preserved of the twins is shown in figure 21 (plate 3, Chap. IV). Figure 19 (plate 2, Chap. IV) shows the appearance of the larger abortus, which contained the smaller nodular embryo only 3 mm. long. The latter is seen at a midpoint near the upper third of the illustration. Both illustrations are practically of natural size. The larger fetus, the external form of which was fairly preserved, had an approximate age of about 48 days, as estimated by the Streeter (1921) curve. Mall noted that the organs could all be outlined, but that they were dissociated, and that the mandibular region had fused with the skin of the thorax. The small nodule, which represents the only remnant of the embryo belonging to the larger chorionic vesicle, contains a large cavity, with thick, fibrous walls, but nothing save epidermis and a remnant of the nervous system could be recognized.


A far more convincing instance of apparent superfetation was found in a specimen of twins donated by Dr. Jane Ross of Binghamton, New York. The fetuses, Nos. 1840 a and b, contained in this abortus are shown in figures 151 and 152. The larger measured 31 mm., but the smaller only 15 mm., indicating respective ages of 63 and 45 days. The chorionic vesicles belonging to these twins, which formed a single mass, are shown in figures 153 and 154. The incised vesicle containing the smaller fetus is shown in figure 154, and the larger vesicle, which is somewhat inverted, in figure 153. Since the latter had been opened and the larger fetus exposed, I at first overlooked the smaller fetus and found it only at a subsequent examination made for the purpose of determining the cause for the peculiar consistency and appearance of this portion of the abortus. The condition of the smaller fetus, which is well revealed in figure 152 under a magnification of 4 diameters, is abundant evidence of the fact that it died a considerable period of time before the abortion occurred. This interval must have been several weeks. This specimen also nicely illustrates the fact that the death of one fetus does not necessarily result in the immediate abortion of it and its vesicle or of the other chorionic vesicle, as is sometimes still assumed.


Through the generosity of Dr. Gustetter, I am also enabled to present reproductions of the fetuses spoken of in his article. They are shown in figures 155 and 156 and from these illustrations it is clear that the smaller of the 2 fetuses probably stopped growth at about the sixth week. After this it became macerated and finally disintegrated, while the larger continued to grow, as in case of the specimen from Dr. Ross. The larger of these fetuses is practically normal in appearance except for the post-partum shriveling. It is approximately 100 days old.


Other specimens in the Carnegie Collection, such as No. 2036 a and 6, well might be included here, for one fetus was grouped as normal and the other as macerated. Indeed, it is a not very rare occurrence to find that the fetuses in a twin pregnancy had to be placed in different groups by Mall and his associates at the Carnegie Laboratory. However, this was not done because such specimens were regarded as instances of superfetation, but because the fetuses, although of the same age, differed in form and appearance. It is interesting that Saniter (1903) also reported a case of two unequally developed tubal conceptuses, one of which was implanted in the isthmus and the other near the fimbria. The former was said to be only of the third to the fourth week, while the latter contained a fetus 4 cm. long. Both chorionic vesicles were said to have ruptured freshly. In commenting on this case of Saniter's, Werth (1904) said that he regarded the question as to whether it was a case of superfetation or merely one of twin pregnancy an open one.


It may be recalled that the occurrence of fetus papyraceus in cases of twin pregnancy also has been attributed in the past to superfetation. Moreover, as stated above, intrauterine death of one or more fetuses belonging to the same litter is relatively common in some mammals. However, since Jenkinson (1913) stated that the allantois and its blood-vessels and also the syncytium are regularly retained at birth in some marsupials, to be absorbed later through the activity of maternal leucocytes, it is evident that one must use caution in judging on the basis of experience in other mammals, especially the lower ones. In some of these the conditions are apparently quite different from those encountered in man. Strahl and Henneberg (1902) also pointed out that in the mole the entire placenta and membranes, as Hubrecht stated, are often retained for a month after parturition. No one would assert that the human uterus shows the same tolerance or the same resorptive power, yet the daily experience of physicians, as well as the literature in obstetrics and gynecology, is replete with instances of retention of the membranes or the entire conceptus long after the death of the fetus. Although the presence of a surviving conceptus in multiple pregnancy materially alters the intrauterine conditions, it also would seem to predispose to retention rather than to hasten the expulsion of the dead mate. That is, the survival of one twin, especially in the earlier stages of development, may depress rather than enhance the factors that lead to abortion.


The impulses arising from the presence of the dead fetus may be counterbalanced or offset, for a time at least, by the presence of the living fetus, and thus tend to prolong the status quo. This would be the case particularly whenever, as in the specimen donated by Dr. Ross, the two chorionic vesicles are fused into a single mass; for then the portion belonging to the dead fetus, even if it forms onehalf of the combined mass at first, soon is outstripped in size by the surviving vesicle, which, in the absence of infection, may continue to grow quite undisturbed, for some time at least; and even in the case of infection of the dead vesicle, prompt invasion of the living does not necessarily occur. Aside from clinical experience, this was indicated also by the experiments of Maffuci (1894) on incubating eggs and on pregnant rabbits and guinea-pigs. The apparent resistance of the young fetus to syphilis, the characteristic lesions of which have not as yet been successfully demonstrated in fetuses much before the second half of pregnancy, would also seem to point in the same direction.


From these considerations it would seem to follow that especially favorable conditions for the production of gross differences would exist in some cases of twin pregnancy. Hence it need not surprise us that these differences have been largely responsible for the quite general belief in the occurrence of superfetation in women. But at present it remains merely a possibility, for the evidence on which this belief rests is wholly inadequate. It is interesting to recall that, in the past, fetus papyracei have also been regarded as examples of superfetation, as illustrated by the specimens reported by Fasola (1887).

Description of Plate

Plate 14

Mall Meyer1921 plate14.jpg


Figs. Fig. 141 - Fig. 142 Hydatiform villi from No. 2250a and 6, shown in fig. 134, plate 12, Chapter VIII. X4.

Figs. Fig. 143 - Fig. 144 Twin conceptuses, both with hydatiform chorions. No. 241 lo and 6. (See Chap. VIII.) X1.35.

Fig. 145. Enlarged fetus from same, showing maceration effects. X2.

Figs. 146-147. Macerated hydatiform villi from the same case. X6.

Fig. 148. Cyema covered with magma. No. 1771. (See Chapter IX.) X2.67.

Fig. 149. Apparent superfetus from a cat. (After Harman.)

Fig. 150. Macerated, distorted normal cat fetus 10 mm. long. (After Kunz.)

Fig. 151. Slightly macerated twin fetus. No. 1840o. X 11.35.

Fig. 152. Pseudosupcrfetus. No. 18406. X2.67.

Fig. 153. Opened, everted vesicle of No. 1840a and incised vesicle of 18406. X0.66.

Fig. 154. Opened chorionic vesicle of 18406 and placcntal area of 1840a. X0.66.

Fig. 155. Twin fetus. No. 20366. X0.66.

Fig. 156. Pseudosuperfetus, No. 2036o, disarticulated by maceration. X2.

Plate 14: Fig. 141 | Fig. 142 | Fig. 143 | Fig. 144 | Fig. 145 | Fig. 146 | Fig. 147 | Fig. 148 | Fig. 149 | Fig. 150 | Fig. 151 | Fig. 152 | Fig. 153 | Fig. 154 | Fig. 155 | Figs. 156 | Chapter 10 Alleged superfetation


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العربية | català | 中文 | 中國傳統的 | français | Deutsche | עִברִית | हिंदी | bahasa Indonesia | italiano | 日本語 | 한국어 | မြန်မာ | Pilipino | Polskie | português | ਪੰਜਾਬੀ ਦੇ | Română | русский | Español | Swahili | Svensk | ไทย | Türkçe | اردو | ייִדיש | Tiếng Việt    These external translations are automated and may not be accurate. (More? About Translations)

Mall FP. and Meyer AW. Studies on abortuses: a survey of pathologic ova in the Carnegie Embryological Collection. (1921) Contrib. Embryol., Carnegie Inst. Wash. Publ. 275, 12: 1-364.

In this historic 1921 pathology paper, figures and plates of abnormal embryos are not suitable for young students.

1921 Carnegie Collection - Abnormal: Preface | 1 Collection origin | 2 Care and utilization | 3 Classification | 4 Pathologic analysis | 5 Size | 6 Sex incidence | 7 Localized anomalies | 8 Hydatiform uterine | 9 Hydatiform tubal | Chapter 10 Alleged superfetation | 11 Ovarian Pregnancy | 12 Lysis and resorption | 13 Postmortem intrauterine | 14 Hofbauer cells | 15 Villi | 16 Villous nodules | 17 Syphilitic changes | 18 Aspects | Bibliography | Figures | Contribution No.56 | Contributions Series | Embryology History

Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)