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Friday, March 28, 2014

Uterine rupture and fetal mummification

Keywords: mummified, rupture, uterus, feline.

During routine ovariohysterectomy in a cat, the surgeon encountered a pregnant uterus containing five normal embryos estimated to be approximately 28 days old. A sixth enlargement, its location indicated by the orange ring in the inset below, contained an embryo that had died recently.


Image size: 888 x 629px  Copright: Dr Robin Bain: psah7423108@hotmail.com

Three mummified fetuses (A above and below as well as B and C below) were found outside the uterus.


Image size: 1203 x 868px

Also outside the uterus, was a fetal femur and a structure (D) that resembled a ovarian remnant, containing corpora lutea. There were numerous adhesions between fetuses A and B and the omentum in the left side of the peritoneal cavity, adjacent to the spleen,  Fetus C was found in the right side of the abdomen, not attached to omentum. The face of this mummified fetus is indicated by a yellow ring in image C.side 2.

Histology of structure D showed that it contained luteal-like cells, supporting the contention that it was an ovarian remnant. Macrophages in the specimen were laden with hemosiderin,  also suggesting a traumatic origin for the structure. It is likely that a fragment of the ovary was torn away during the incident that traumatized the rest of the tract.

The dead embryo is shown here, just above the scale and between the other embryos. The other embryos were viable at the time of surgery. On the right side, one of those embryos has been exteriorized, showing its large yolk sac, typical of this stage of gestation.


Image size: 1159 x 553px

Close inspection of the uterus did not reveal any site of rupture that may have released the fetuses into the abdomen. This is not surprising because the uterus has a remarkable ability to heal by first intention after rupture; perusal of the literature indicates that it is not uncommon to find no evidence of a rupture site.

This cat had produced a litter of three or four kittens (the number is uncertain) within the six month period prior to surgery. It is possible that the mummified kittens encountered here, were part of that litter. However, as is evident here, the uterus healed uneventfully after rupturing, and five kittens were currently in gestation. Therefore, the mummified kittens could have been part of any litter that had previously developed in this cat.

A brief summary of extra-uterine pregnancy in various species:

There are two basic forms of extra-uterine pregnancy: primary and secondary. Primary extra-uterine pregnancies are thought to arise from fertilization that occurs in an extra-uterine environment. Secondary extra-uterine pregnancies arise from zygotes that form within the reproductive tract then escape into the abdomen. Although extra-uterine pregnancies are well described and fairly common in women, there is still doubt about the possibility of primary genesis of such pregnancies. However, it is known that extra-uterine pregnancies do form after retrograde movement of tubule pregnancies, rupture of the fallopian tubes (uterine tube/oviduct) after tubule pregnancies and rupture of the uterus in uterine pregnancies. Embryos may also escape into the abdomen when there is incomplete healing after cesarean sections; this has been well documented. True extra-uterine pregnancies are most common in humans. These may even go to term, producing live babies. However, extra-uterine pregnancies of a similar nature also occur in sub-human primates. 

Extra-uterine pregnancies in humans are relatively easy to explain in comparative terms because human embryos show aggressive implantation or nidation providing an ability to implant on surfaces other that the endometrium. Importantly too, human embryos are not required in the uterus for pregnancy recognition. In most domestic animals (apart from carnivora) the presence of the embryo in the uterus is essential to block luteolysis and allow the continuation of pregnancy. By contrast, tubule pregnancies can last for many weeks and as mentioned, extra-uterine pregnancies can even go to term, all in the absence of endometrial signalling.

Extra-uterine pregnancies have also been shown in rabbits, mice, rats and hamsters, all of which have placentation that is more intimate than that of domestic animals. That suggests that they may implant in the abdomen when embryos of domestic species cannot. Indeed, this is the case because embryos of these species can, with varying success implant in muscle, sub-capsular organ tissue, the anterior chamber of the eye and even in testicles! It is not surprising then, to see fairly common reports of extra-uterine pregnancies in rabbits. These may develop well into late gestation but none of the rabbit pregnancies have been known to produce viable neonates (via cesarean section). It is somewhat perplexing however to see how frequently these are reported and then to try and reconcile that with abdominal injury and secondary extra-uterine pregnancies. Perhaps some of these pregnancies arise from retrograde movement of embryos after fertilization in the fallopian tubes. 

Almost certainly, extra-uterine pregnancies in ruminants, mares, bitches, sows and cats (all of which have been reported) are secondary in nature i.e they are the result of uterine rupture. None of these animals have placentas that has been shown to implant on any surface other than the endometrium. In the case reported here and elsewhere in LORI, extra-uterine pregnancies are almost certainly the result of uterine rupture. 

For additional detail see Corpa, J.M. 2006. Ectopic pregnancy in animals and humans.Reproduction.131: 631–640) and the numerous papers that have reviewed in that excellent article.