Placentome variation. Ovine

 

Ovine placentation: placentome variation

Key words: multiplex, placenta, sheep, ovine

Sheep usually have about 80 to 90 placentomes with little variation. Caruncles are already present in the non-pregnant uterus (even before birth) and form future attachment points for cotyledons. The combination of caruncles on the maternal side and cotyledons on the fetal side form joint structures known as placentomes. Caruncles determine the sites for cotyledons on the surface of the chorion. Caruncles are not usually concave at the time of conception but develop into concave structures in most cases as pregnancy progresses. In some cases however, flat or even convex caruncles develop. As discussed below, this may be influenced by stress, nutrition and multiple fetuses.  

Figure 1. An image of a normal fetal-placental unit from a singlet pregnancy towards the end of gestation. Image size:1000 x 750px  

Figure 2. A cotyledon being withdrawn from a caruncle in this pregnancy. Although the majority of caruncles were concave in this pregnancy, a few caruncles (not shown) were indeed convex as occurs in cattle. Viewing the image at its highest resolution (right click on image) reveals the fine structure of the fetal villi. Image size: 4764 x 3456px

Figure 3. An area of caruncles with the cotyledons removed in most cases. As demonstrated by the small caruncle close to the center of the image, there can be considerable variation in their size. Image size: 4800 x 3456px

In times of nutritional stress, fewer placentomes are formed than otherwise. This has been shown in controlled studies on stressed and energy-deprived ewes. Interestingly, this not only affects the number of placentomes but their shape as well. In such states, some placentomes became flatter and even become bovine-like as alluded to above. Interestingly, these changes also occur in apparently normal pregnancies. Therefore one should exercise caution in studies of this nature. It not clear if caruncles established as concave can change their shape as pregnancy progresses but some data do suggest this may occur. i.e. 

Alexander G. (1963) reported that "....there was a marked tendency towards cotyledonary eversion; in nine out of ten placentae at both the 95th and 114th day the maternal tissue almost completely enveloped the foetal cotyledon, but at 135 days, the foetal tissue tended to surround the maternal in eight out of fourteen placentae, much as in the normal bovine cotyledon illustrated by Andersen (1926)."  

From these data and those reviewed by Vatnick et al, 1991, the author has a drawn a representation of  this situation:

Figure 4. The marked tendency towards cotyledonary eversion seen in some ovine pregnancies. These placentomes have been classified as types A to D. Type D is the most bovine-like of these. The green arrow questions whether this transformation occurs as pregnancy advances or if placentomes develop this architecture from the outset in some pregnancies. Interestingly, using a mathematical model, type D placentomes appear to the most efficient of all these forms of placentation. Using similar modeling, it has also been determined that ruminant placentation is highly efficient; 5 to 10 times more so than the diffuse, micro-cotyledonary placentation found in mares. Image size: 800 x 780px

This author has often wondered how essential the inter-placentomal areas are in maternal-fetal exchange in ruminants. As reviewed by Wooding and Burton (an excellent resource on placentation) there are small areolae over the mouths of the uterine glands in these areas but other than that, very little fetal-maternal exchange occurs in those areas. In fact, the inter-placentomal areas account for less than 5% of the total exchange at the end of ruminant gestation.

Figure 5: An ovine pregnancy approximately 60 days duration showing some caruncles with a bovine (type D) appearance while others are clearly concave developing into the most common form of placentomes (type A). Right click to read labels and see in full size. Although the dark black areas on the endometrium are labeled as "Degenerate caruncles", this author is not at all certain if that is correct. Image size: 2599 x 1572px

Selected references:

Alexander G. 1963 Studies on the placenta of sheep J. Reprod Fert. 7:289-305

Vatnick I. et al. 1991. Growth and metabolism of the placenta after fetectomy in twin pregnant ewes. J. Development Physiology 15: 351-356

Vonnahme, K. A.  et al. 2006 Placentomal differentiation may compensate for maternal nutrient restriction in ewes adapted to harsh range conditions J. Anim Sci 84:3451-3459

Wooding, P. and Burton, G. 2008 in Comparative Placentation: Structures, Functions and Evolution. Pub. Springer eISBN: 9783540787976

Evisceration during late gestation

Keywords: ovine, gestation, late, accident, pregnancy, sheep

The image below shows a Texel ewe, estimated to be ~135 days post breeding. This animal was found dead in the pasture with no prior signs of debility. The intestines had eviscerated through a tear in the dorsal vagina.

Image size: 1667 x 2500px

This ewe was one of six that died suddenly during late gestation. In each of three cases examined by the author, there was a single rupture in the dorsal wall of the vagina, several centimeters caudal to the cervix. Intestines had eviscerated through the tear. In the six cases reported by the farmer, the pregnancies were advanced, approximately 135 to 145 days. The fetuses were twins in all cases and all appeared to be normal. 

The image below shows the location and nature of the rupture and evisceration.

Image size: 2003 x 1208px

The following image shows one of the fetal lambs lying in situ, in the left uterine horn.

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This condition is very poorly documented in the literature, it's etiology unknown. Sporadic cases have been reported in the United Kingdom. Characteristically, all ewes eviscerated their intestines through a single tear in the dorsal vaginal wall. Most ewes were found dead, others euthanized. In one case, a failed surgical repair was recorded.

As one practitioner described to the author: "In one case, the shepherd was present and the ewe was standing and not straining when all of a sudden intestines began to pour from the vagina."

Affected ewes show neither vaginal prolapse nor straining prior to evisceration. The incidence may be as high as 5 per cent in some flocks. It has been associated with excessive body condition and feeding of concentrates but some ewes are in poor condition when this occurs. Interestingly, it has not been reported in primiparous ewes. Therefore, one is left wondering if the condition may be associated with previous lambing injuries. Perhaps tearing is precipitated by abdominal pressure increase due to rapid fetal growth, multiple fetuses and distended abdomens after high feed intake.

There is no evidence that sadism is involved in this condition.

Selected references:

Knottenbelt, D.C. 1988. Vaginal rupture associated with herniation of abdominal viscera in pregnant ewes. Vet. Record  122:453-456

Scott, P.R. 2015. Sheep Medicine 2nd Edition. pg 45 ISBN-10: 1498700144 ISBN-13: 978-1498700146

Term uterus and maintenance of pregnancy

Keywords: ovine, sheep, placenta, corpus luteum endocrinology, pregnancy

An illustration of a term uterus and the ovaries.  Although this was a triplet pregnancy, the ovaries were very small (arrows) and contained corpora lutea that were significantly smaller than those in cycling ewes. They appeared to be in a state of regression similar to that shown on the lower left inset, a CL from another term ovine pregnancy.

Image size: 1499 x 1691px

In ewes, the corpora lutea are only essential for the maintenance of pregnancy in the first third of a 145 to 150 gestation. After about 60 days (with some variance) neither ovariectomy nor luteolyic treatment with prostaglandins will cause abortion. This is because pregnancy is maintained by the placenta. This situation is distinctly different to that in goats where luteal tissue is essential throughout pregnancy.

With single, twin and triplet lambs in one study, neither gestation length, birth weights nor incidence of dystocia were affected by ovariectomy at 70 days of gestation. The lack of dystocia is not surprising, because ovine corpora lutea are not essential sources of relaxin during pregnancy (as they are in pigs); that role falls to the placenta in sheep.

Although corpora lutea are present at the end of gestation and actively contribute to serum progesterone concentrations,  the essential role of luteal tissue in late gestation remains an enigma.

References:

Al-Gubory,K.H. et al 1999. Effects of luteectomy on the maintenance of pregnancy, circulating progesterone concentrations and lambing performance in sheep. Reprod.Fert.Devel. 11:317 - 322 

Bryant. G and Chamley, W.A. 1976 Plasma relaxin and prolactin immunoactivities in pregnancy and at parturition in the ewe. J. Reprod Fert. 48:201-204

Triplets and absence of freemartinism

Keywords: ovine, sheep, triplets, freemartin

With the high incidence of multiple births, it is obvious that freemartinism is not usually a significant problem in sheep. In this set of triplets, two lambs were male and the third a female.

As is the case in bovine freemartinism, the lambs shared a common chorion, yet there was no evidence of suppression of the müllerian system in the female. See the uterus of the female at lower right. The males were normal and both had scrotal testes.

Image size: 1540 x 2343px

The reason for a comparative lack of freemartinism in animals other than cattle is not known. Nevertheless, freemartinism does indeed occur in sheep, especially is large "litters" of four or more. However, in most studies the incidence is only about one percent in polytocous female lambs. Interestingly, freemartin lambs are highly masculinized; more so than bovine freemartins and often have gonads that resemble testicles, lacking oocytes altogether. Apparently, the müllerian system is so severely suppressed in some ovine freemartins that it is altogether absent.

Incidentally, freemartinism has been reported in many species but it does not appear to occur in horses.

Selected references:

Padula A.M. 2005 The freemartin syndrome: an update. Anim. Reprod. Sci.87:93–109

Smith K.C. et al 2003 Morphological, histological and histochemical studies of the gonads of ovine freemartins.Vet Rec 152:164-169.

Vaginal tear in a ewe; post prolapse

Keywords: ovine, ewe, sheep, prolapse, vagina, retainer, rupture, pregnancy

Image size: 1037 x 691px

Sequel to the use of a retaining device (upper left in the image) used to keep vaginal mucosa in-situ after returning it to the pelvis. The inset image shows the pregnant uterus within the abdomen.

Below; the location and size of the tear in the vagina:

Image size: 869 x 792px

Plastic devices  are often used to retain vaginal mucosa in the vaginal lumen after late gestation vaginal prolapse. Pressure from the cranial edge of the device will occasionally cause pressure necrosis of the cranial vaginal, allowing evisceration to occur. Death follows rapidly.

To prevent this problem, this author uses epidural anesthesia followed by a Buhner-type closure. Farmers who cannot avail themselves of this treatment and are forced to use these devices, should probably thicken the cranial edge of the device by whatever means possible. Alternatively, special "prolapse trusses" (commercially available) can be used.

Ovine pregnancy at 25 days

Keywords:  ewe, sheep, pregnancy, embryo, membranes, ovine

Image size: 1160 x 647px

A labeled image of an ovine embryo about 25 days old. The author acknowledges the help of Dr. Glenda Wright (Embryologist; Atlantic veterinary college) in accurately documenting the structures within the embryo.

Co-twin ovine embryos

Keywords: twins ovine embryos, sheep, placenta

Image size: 2032 x 1574px

Twin ovine embryos about 23-25 days old. The embryos originated from twin ovulations in the right ovary. The corpora lutea visible here would be required to maintain pregnancy for the first third of gestation; after that the ewe could even be ovariectomized because the placenta would maintain pregnancy. This is unlike the situation in goats where the corpora lutea are required throughout pregnancy.