Paper - Abdominal pregnancy in animals with an account of a case of multiple ectopic gestation in a rabbit (1932)

From Embryology
Embryology - 10 Apr 2021    Facebook link Pinterest link Twitter link  Expand to Translate  
Google Translate - select your language from the list shown below (this will open a new external page)

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)

Eales NB. Abdominal pregnancy in animals, with an account of a case of multiple ectopic gestation in a rabbit. (1932) J Anat. 67: 108-117. PMID 17104404

Online Editor 
Mark Hill.jpg
This historic 1932 paper by Eales describes ectopic pregnancy in the rabbit.

Modern Notes: ectopic pregnancy in the rabbit

Rabbit Links: 2009 Student Project | Category:Rabbit | Animal Development
Historic Embryology - Rabbit 
1889 Uterus and Embryo | 1905 Normal Plates | 1905 limb veins | 1908 Pancreas | 1908 Pharyngeal Pouches | 1908 intestinal diverticula | 1909 Lymph glands | 1918 Pituitary | 1929 ovulation | 1931 prochordal plate | 1935 Oocyte | 1935 Somites | 1964 Placentation
Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic" (textbooks, papers, people, recommendations) 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, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Abdominal Pregnancy in Animals, with an Account of a Case of Multiple Ectopic Gestation in a Rabbit


Lecturer in Zoology in the University of Reading


Abnormalities in the position of the developing embryo are by no means uncommon in the human subject, but are rare amongst other Mammals. The present account records the presence of four foetuses in the abdominal cavity of a tame rabbit. The doe was a black and white English rabbit born in January, 1930, and at the time of dissection was 1 year and 10 months old. She had bred three times, but each time only one young rabbit was born dead. No signs of ill health were noticed by the owner. The last birth was in February, 1931, when the mother produced one abnormally large dead foetus. She had been a successful foster mother to litters of four and two respectively. The brother of this doe is sterile; the parents were apparently normal.

The rabbit was one of twenty-five dissected by the elementary class. It was observed that the abdomen was enlarged, and a hard lump could be felt in the right inguinal region. The students who dissected the specimen were warned to look out for foetuses, but did not expect to find these in the abdominal cavity! On opening the cavity, two ovate tumour-like bodies became visible. The larger of these lay in the right posterior portion of the coelom, lateral to the bladder and vagina, and the smaller was situated under the left side of the arched diaphragm, pushing the stomach in a posterior direction and the liver over to the right. Each was held in place by from five to eight narrow strips of tissue, acting as anchoring processes and bearing small blood vessels. There was no marked vascularisation of cither the “tumour”? or its supports; both were pale in colour. The two bodies were removed and preserved for examination, and the students were supplied with another rabbit so that the reproductive organs might be left undisturbed. In addition to the two large bodies, three smaller structures were found floating freely in the coelom. These were also removed and preserved.

The rabbit was very fat but exhibited no signs of disease. The heart was rather large. The lungs were normal and no abnormalities were apparent in any of the endocrine glands. The ovaries were large, the right ovary measuring 13 x 7mm. and the left 15 x 9mm. The right ovary had two corpora lutea and two black swellings full of liquid, and the left ovary eight corpora lutea and four similar blackened vesicles. The funnel of the left Fallopian tube lay in its normal position, but on the right side the funnel was wholly anterior to its ovary. Both funnels were abnormally large, measuring 13 mm. in length on the right and 19 mm. on the left. The Fallopian tube was also of wide calibre, being at first 4 mm. in diameter and highly vascular. A seeker passed readily through the funnel into the tube, which enlarged to about 6 mm. diameter as it neared the uterus of its side. Both tubes showed undoubted signs of degeneration at this point, the walls becoming fatty, soft, and so thin-walled as to be transparent. The whole of the broad ligament was loaded with fat and it was difficult to isolate the tube, or to determine whether it had actually burst. The opening of the tube into the uterus, the uterus itself and its aperture to the vagina were normal on both sides. The peculiarities of the genital organs and their ducts were thus the large size of the ovaries, their blackened follicles, the enlargement of the funnels and Fallopian tubes, and the degeneration of the posterior portions of both tubes.

The five foetal remains were next examined. The largest, which lay in the right inguinal region, measured 55 mm. in length, 46 mm. in width and 32 mm. in thickness. It was fastened to the body wall by eight strips of connective tissue, whose small blood vessels were apparently in communication with the | ilio-lumbar arteries and veins, but the vessels were so slight that it was difficult to determine this with accuracy. Two membranes covered the foetus, obviously the foetal chorion and amnion. There was no amniotic fluid. Within lay a fully formed mummified foetus, whose right side had been absorbed so that the skeleton was exposed, but whose left side still had flesh on it. The foetus was hard and stony, its bones were very well ossified, and as dark in colour as if stained with alizarin. It lay curled up, with the head close to the right side of the pelvis, and the right arm folded with the hand directed dorsalwards (sce figure). The length from nose to tip of the tail along the curve of the back was 152 mm., which is the length of a full-term foetus of average size. The skull was almost completely ossified, and the incisor and premolar tecth were plainly visible. The eye had sunk in the orbit. The vertebral column, with well-ossified paired arches, showed through the membranes before the removal of the latter. Seven ribs, somewhat crushed, could be seen. Radius and ulna were separable. The left side of the foetus, which lay in contact with the dorsal abdominal wall, had undergone much less absorption than the right side. The bones were here covered with hard flesh, and the only parts of the skeleton visible on the surface were the left ilium and hind-limb and the toes of the left foot, which lay over the left side of the occiput. The much twisted umbilical cord was lying on the surface. The remnant of the placenta was of the usual flattened shape, and measured 23 mm. long, 19 mm. broad and 8 mm. thick. Only a small portion of it is seen in the figure as it curved round towards the left side of the foetus.

It is remarkable that although this foetus had had no separate existence, its bones were more completely ossified than in the early post-natal condition. For example, in a 2-day rabbit the scapula measured 18 mm. in length, but of this length 6 mm., or one-third, was cartilaginous suprascapula. The bony part was therefore 12 mm. long. In the mummified foetus the length is 17 mm., of which 15 mm. is bony and only 2 mm., or one-eighth, is cartilage. Even allowing for some absorption of the cartilage, this represents a higher proportion of bone to cartilage than is usual in the foetus.

The second foetal mass, which lay under the diaphragm, measured 42 mm. long, 40 mm. broad and 20 mm. thick. Like the first, it was attached to the body wall by narrow strips of tissue containing small blood vessels, and the membranes covered it. It lay on its right side, with the left hand flexed towards the face. Along the curve of the back, from nose to tail, it measured 128 mm. and was probably between 25 and 380 days old when it died. The maceration of this foetus was much less advanced than in that first described. The muscles and skin were comparatively soft, and even on the left exposed side a considerable amount of tissue had to be cleared away to show up the skeleton. As regards age, this foetus was younger than the former foetus. It was smaller, and there was a larger proportion of cartilage in its skeleton. Thus the scapula was 13 mm. long, 10 mm. was bony and 8 mm. cartilaginous, or approximately one-quarter of the length was cartilage. Compare these figures with those for the first foetus. This specimen had no trace of a placenta, and the umbilical cord was not visible on the surface.

The largest foetal mass stripped of its membranes and dissected superficially to show the position of the parts of the body. All the bones figured could be seen through the remains of the skin, and the muscles of this side had almost entirely disappeared. The backbone is indicated by the neural arches in so far as these were exposed by maceration. Bone lined, cartilage dotted. pl. placenta. Drawn from a photograph. x 2 approx.

The three floating bodies, which were soft and not at all mummified, were about 20-25 mm. long, 20 mm. broad and less than 10 mm. thick. Two contained small foetuses about 10 mm. long, enclosed by their membranes and with their placentae. Although maceration had begun, it was still possible to trace the foetal form, to shell it out of its membranes and to determine its relationship to the placenta. Some ossification of the skeleton had occurred. The third body appeared to be a dermoid cyst. It contained three masses separated by fibrous tissue. Each contained calcareous concretions, which were effervescent in hydrochloric acid. There was no trace of a foetus or placenta, and this body differed from the others in being foetid.


Although ectopic pregnancy has been recorded many times in the human subject, very few authors have reported it in other Mammals, despite the large numbers of animals dissected. Thus, the Index Catalogue of the Library of the Surgeon-General’s Office, United States Army, devotes over a hundred columns to lists of papers on the subject in human beings, and only half a column to its occurrence in animals. A study of the literature does not greatly augment this short list, and the records refer to a small number of species only, mostly domestic Mammals. There are records for the hare, rabbit, cow, ewe, sow, cat and bitch, mostly one for each species, except in the rabbit and hare. Those in the rabbit, it may be noted, are frequently in animals employed for experimental purposes.

The earliest account of ectopic pregnancy in animals is given by P. Rommel in a Physico-medical Discourse, published at Ulm in 1680, and refers to the hare. A very large hare was brought in by a huntsman, who found two large spheres in the abdomen close to the stomach, among the folds of the intestine. Rommel made an incision through the membranes surrounding one of these growths and found in it a compact hairy mass, which he thought at first was similar to the hair balls found in the stomachs of goats, oxen and horses. But further investigation disclosed a perfect little hare. He says that he believes this hare developed outside the uterus and near the stomach, as was described by the huntsman. He then proceeds to discuss a number of cases of conception in cavities of the body other than the uterus (stomach, intestine, scrotum, Fallopian tube, ete.), nearly all of which are incredible, and concludes that it is not impossible that his little hare may have been conceived outside the uterus, and compares this phenomenon with the presence of parasites in various parts of the body. He states that several anatomists have testified to the occurrence of tubal pregnancies!, and adds that as it is now held that conception in the first place is in the tube, this is not extraordinary. Indeed a foetus has been seen attached to the outside of the tube and consequently conceptions must be possible in cavities of the body other than the cavities of the generative ducts.

1 Presumably in Man as no animal is mentioned.

In 1685 Buissiere, after describing a case of retention of the foetus after ectopic pregnancy in a woman, adds an account of a similar occurrence in a hare. Like Rommel’s specimen, the animal was brought to Buissiere by huntsmen, who had found numerous young in the abdomen. Buissiere examined the specimen and described the young, still within their membranes, lying in the coelom and having no other connection with the uterus than the placental attachment. He did not, however, mention any rupture of the uterus, and it is not clear if the foetuses were actually attached when he saw them.

It is not surprising that vague and fantastic theories were built around such rare and monstrous foetations. Some refused to believe in them and scoffed at them as miracles; others accepted and attempted to explain them, claiming, as Rommel did, that gestation could occur in parts of the body other than the generative organs. Even as late as the early nineteenth century, when the subject was again brought to the notice of the medical and anatomical world by records in human beings and animals, it was believed that the foetus could implant itself on the abdominal wall by means of a placenta, and develop normally in that position. Several records in the ewe (Simonds) and the hare (Dohrn, Dartigolle) were described, and at the end of the century cases were discussed in the medical societies of London and Berlin, and raised the whole question of abnormal pregnancy in Man and animals, with the result that many of the old errors were swept away, and the ground cleared for a more adequate explanation of the abnormalities recorded. It is unfortunate that most of the accounts relating to animals during the period 1890 to 1910 are in medical journals, where the zoologist is not likely to meet with them.

In 1898 Drs Pembrey and Bellingham Smith exhibited at a meeting of the Obstetrical Society in London five foetal sacs found free in the abdominal cavity of a rabbit kept for experimental purposes. Four of the sacs contained a full-term foetus, the fifth carried four full-term young. A more detailed account in 1904 described the case as one of multiple utero-abdominal pregnancy, on the evidence that “the uterus showed evidence of a former rupture in the shape of an old scar at the junction of the two uterine horns.” To the comparative anatomist it is clear that these authors are confusing the vagina of the rabbit with the uterus of the human female, for the uterus of the rabbit is paired, not median. The case appears to be one of ruptured vagina at parturition, probably owing to the quadruple gestation sac described above. This interpretation receives confirmation from the equality in age, and freedom from attachment of the foetal sacs. Sir John Bland Sutton, however, in his Purvis Oration for 1904, makes Pembrey and Smith’s case the main support for his thesis that all apparent abdominal pregnancies are secondary, having burst out from either the Fallopian tube or the uterus into the coelom. In the human subject tubal pregnancy is the common cause of the extrusion and in other Mammals a ruptured uterus.

In Germany, at the beginning of the twentieth century, several ectopic pregnancies were described in animals, and aroused such interest that an attempt was made to bring about the condition experimentally. Wolff (1902) claimed to have found primary abdominal pregnancy in a rabbit, whose single full-term foetus was attached by a vascular network to the spleen and stomach. Former abdominal foetuses had been found free in the abdomen, and because this foetus was fixed, he regarded it as a true case of abdominal placentation. But his specimen was a rabbit which had been operated on some time before the finding of the foetus. A piece had actually been removed from the uterine wall for experimental purposes. The case has therefore all the symptoms of artificial utero-abdominal pregnancy. Another account of supposed primary abdominal placentation was published in a German Gynaecological Journal by Kamann in 1903. The specimen was also a rabbit, and contained one foetus attached to the omentum by a pedicle. But re-examination of the specimen showed that this case, like the preceding one, was due to a ruptured uterus and extrusion of the foetus, for the uterus exhibited the scar of a former rupture. Later, Kamann withdrew his original explanation, and substituted for it: “Apparent abdominal gestation in the rabbit, after primary uterus rupture.” A third example in the rabbit occurred in a specimen used for experiment, and this was described by Henneberg (1903) and Happe (1903). The right uterus had been ligatured 3 days after copulation, and 8 days subsequently the animal was killed. Autopsy revealed four normal foetuses developing in the right uterus. On the left side there was an open fistula and beyond it one normal foetus in utero. The number of fresh corpora lutea corresponded to the number of young in the uteri. But lying in the body cavity were three dead foetuses from 6 to 9 cm. long, enclosed in a single membrane and attached by bands to the wall. These obviously belonged to an earlier gestation, and the ruptured left uterus suggested that they had reached the coelom through the fistula. The authors did not attempt to explain how the foetus developing in the uterus had managed to dodge the opening of the fistula during its passage along the uterus, nor why the rupture had remained unhealed. The most interesting case was an experimental one in the rabbit, described by Sittner in 1903. He took a rabbit which was 8 days’ pregnant, opened one uterus by making a slit 1 cm. long, and hooked out into the abdomen a foetal sac 7-5 mm. in length. The uterus was then sewn up, and gestation proceeded normally. After 33 days two normal living young were born. The rabbit was then killed, and dissection revealed four foetuses in the coelomic cavity. One of these had attached itself to the body wall. Its old placenta was free, and the anchoring strands represented new tissue. Sittner thought that this was a case of secondary abdominal pregnancy, as it undoubtedly was. He suggested that three of the foetuses escaped through the funnel of the Fallopian tube into the coelom by an antiperistaltic action of the uterus.


Five explanations have been given by authors to account for the presence of foetuses in the abdomen of a living animal. These are:

  1. Genuine abdominal pregnancy, by the formation of a placenta on the peritoneal lining. This is an old view, and was held before the process of conception was understood.
  2. Ovarian pregnancy, in which the egg is presumably fertilised before leaving the ovary, and develops there. Many human ectopic pregnancies have been thus described.
  3. Tubal pregnancy, resulting in rupture into the abdominal cavity. Here the fertile egg forms a placenta on the wall of the Fallopian tube or funnel, instead of on the wall of the uterus. The tube has limited powers of expansion and bursts sooner or later, expelling the foetus. The latter may retain its membranes, and may remain attached to the wall of the tube by its placenta and cord. If so, it will go on developing in the abdominal cavity and will make abdominal connections of a secondary nature. If, on the other hand, the placenta breaks away at the time of rupture, the foetus will die in the abdomen owing to the cessation of its nutritive supply, and will float freely in the cavity. The cause of the primary tubal attachment is not known. In animals producing many young at a birth, the uterus may be already fully occupied when the last fertile egg comes down. This does not apply, however, to the human subject, where tubal pregnancy is the most common abnormality of placentation. Retention of the dead foetus is always associated with absorption of its soft parts, and mummified foetuses have been found more than 20 years after gestation in women.
  4. Normal uterine pregnancy resulting in rupture before parturition. This occurs in animals only, and may be brought about by twin, triple and quadruple gestation, where several foetuses within one set of membranes occupy the uterus in a region adapted for bearing one. The strain on the uterine wall may result in its rupture with results as in (8) above.
  5. Normal uterine gestation, with anti-peristaltic uterine contractions of sufficient strength to drive the foetus backwards along the tube and through the funnel into the abdominal cavity. This is merely a theory and has no evidence in support of it.

Of the five interpretations which have been suggested to explain abdominal foetation, there are no authentic cases of (1) and (2), and no evidence is available for (5). Supposed cases of abdominal placentation have proved to be secondary in nature, and supposed ovarian pregnancy is usually tubal, with subsequent attachment close to the ovary. Doran, who had seen many specimens of abdominal foetuses, wrote as long ago as 1893: “‘ When some observer can demonstrate to us a specimen where a foetus as minute as that which I now exhibit?, but recent and entire, is to be seen lodged in a true gestation sac inside the ovary or on the peritoneum away from the tube, then we shall begin to believe in primary ovarian and abdominal gestation.” The third and fourth explanations, i.e. ruptured tubal or uterine pregnancies, are the only ones for which there is direct evidence. In the human subject the tubal type is not uncommon, and Tait (1892) described a case in which the foetus burst the tube at 10 weeks, as evidenced by the mother’s symptoms, but retained its connection with the tubal placenta so that it was able to continue its development in the coelom. A ruptured uterus in woman does not allow of abdominal development, because the haemorrhage following the rupture is fatal to the mother. Hence human cases of abdominal development are of necessity tubal in origin. In animals, on the other hand, the cases recorded previously have all been utero-abdominal in nature.

The present case differs from all the earlier ones in two particulars. Firstly the evidence points to tubal pregnancy in an animal. This is suggested by the enlargement and rich vascularisation of the Fallopian tubes, the fatty degeneration of their posterior portions and the absence of any scar on the uteri. The fact that there is no trace of placental tissue on the inner wall of the tubes is no evidence against this view, since the last pregnancy occurred 9 months previously and placental tissue is readily absorbed. Secondly the dead foetuses are of different ages and exhibit varying degrees of maceration. This suggests that they belong to separate pregnancies, and this is the first case in which repeated abdominal foetation has been recorded in an animal. The two smallest foetuses are about the same age. Each is approximately 10 mm. in length and has its own placenta. These two probably broke away together from the maternal tissues at an age of about 12 days, and died in the abdominal cavity owing to the stoppage of their food supply. The softness of the foetal sacs and the very slight degree of absorption point to a recent rupture. The two large foetuses have undergone about 25 days and full-term development respectively. This can be deduced from their size and the degree of ossification of their bones. The largest foetus evidently lived in the abdomen beyond the full term of 30 days. In size, even in its mummified and partially resorbed state, it is as large as a new-born rabbit. Its bones, however, are older than this, as ossification has proceeded well beyond the parturition period (see p. 109). The marked difference in the absorption of the soft parts indicates that these two large foetuses belong to two gestation periods, so that three such periods are represented by the four foetuses. Whether these three correspond to the three known pregnancies of the animal we cannot now determine, but as there were only three pregnancies, it seems likely that each produced one stillbirth (see p. 108) and one or more abdominal foetuses. There is apparently nothing to account for the abnormal foetation. The stillborn young found the right way out through the uteri and vagina, so that closed ducts were not the cause. Dissection also showed that these were normal and patent. There was no record of ill health, of over-production of young, or of more than one young in a single set of membranes stretching the ducts unduly. The stillborn young were presumably uterine gestations. Did the presence of dead foetuses in the abdominal cavity cause their death? Were the tubes originally too wide, so that the fertile eggs settled down prematurely there? Or did the luteal and pituitary hormones act too rapidly, stimulating attachment before the uteri were reached, thereby widening normally slender tubes? Nothing in the specimen gives any clue to the answers to these queries.

1 One inch in length.

The two youngest foetuses formed no abdominal attachments, and from this it can be inferred that the placental connection severed itself at the same time as the tubal break, so that the little rabbits died there and then. The two — large foetuses, however, were anchored by strips of living tissue to the abdominal wall. This implies that they lived for some time after extrusion from the tubes, and as a consequence must have remained attached by their placentae and umbilical cords to the tubes. From their position it is almost certain that they came from different tubes. The anchoring tissue was probably formed before they died. Death resulted from their inability to find the correct way to the outside world, and not from an interruption of their nutritive supply from the mother.


An English doe rabbit, which had borne three dead young at different times, was found on dissection to contain the macerated remains of four foetuses in the coelom.

Two foetuses had died at about 12 days, and with their membranes and placentae, floated freely in the coelom. Two were attached to the abdominal wall by secondary anchoring processes.

The condition of the Fallopian tubes suggested that the four foetuses were tubal pregnancies which had burst out into the coelom. Two had broken away completely, and two had retained their placental connections up to 25 days and beyond full term respectively.

The chief points of interest in this case are that both tubal and uterine pregnancy had occurred, and that foetuses of three stages of development were present in the abdomen at the same time. This is the first record of tubal pregnancy in an animal, and of repeated extrusion of foetuses into the abdominal cavity. Abdominal Pregnancy in Animals 117


BuIssiERE (1685). Nouvelles de la République des Lettres, Amsterdam, Article 6, t. v, pp. 994-7.

DaRTIGOLLE (1880-1). Bull. Soc. @anat. et physiol. de Bordeaux, vol. 1, p. 15.

Dourn (1861). Archiv f. pathologische Anatomie und Physiol. und fiir klinische Medizin, Bd. xx1, p. 249.

Doran, A. (1893). Trans. Obst. Soc. Lond. vol. xxxv (4), pp. 222-39.

Harpe, H. (1903). Anat. Hefte, Wiesbaden, Bd. xxu, pp. 601-19.

HENNEBERG (1903). Deutsche med. Wochenschr. Leipzig und Berlin, p. 260.

Index Catalogue of the Library of the Surgeon-General’s Office, U.S. Army (1908). References to papers on human and animal cases of ectopic pregnancy.

Kamann, K. (1903). Zeits. f. Gyndk. Leipzig und Berlin, Bd. xxvu, pp. 515-17.

Pemsrey, M. S. and BELLIncHaM SmiTu, G. (1898). Trans. Obst. Soc. Lond. vol. xu, pp. 253-6.

—— (1904). Trans. Obst. Soc. Lond. vol. xvi, p. 283.

RommeEt, P. (1680). De foetibus leporinis extra uterium repertis. Ulmae.

Suaw, W. V. (1904). St Mary’s Hospital Gazette, London, p. 94.

Srmonps (1842-3). Trans. Vet. Med. Ass. vol. 11, p. 492.

Srrrver, A. (1903). Arch. f. Gynaek. Berlin, Bd. Lx1x, pp. 688-701.

Srrauu and HENNEBERG (1902). Anat. Anz. Bd. xx1, pp. 644-50.

Sutton, Sir Joun Bianp (1904). Lancet, London, vol. 1, pp. 1625-7.

Tarr, Lawson (1892). Trans. Obst. Soc. Lond. (3), vol. xxxtv, pp. 192-8.

Wotrr, B. (1902). Zeits. f. Geburtsch. u. Gyndk. Stuttgart, Bd. xivmt, p. 171.

Note. The author has not seen the papers by Dohrn and Simonds. After the manuscript of the above was submitted for publication, a paper on Abdominal Pregnancy in a Cat, by Dr R. H. Hunter, appeared in J. Anat. vol. txv1, No. 2, pp. 261-3.

Cite this page: Hill, M.A. (2021, April 10) Embryology Paper - Abdominal pregnancy in animals with an account of a case of multiple ectopic gestation in a rabbit (1932). Retrieved from

What Links Here?
© Dr Mark Hill 2021, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G