|Domestic ewe with mouflon offspring from embryo transfer (Courtesy Dr. T.D. Bunch).|
General gestational data
Keisler (1999) has provided a detailed review of the reproductive parameters of domestic sheep and goats. The reader is also referred to the Chapter on Cretan Goat. That species' reproductive aspects have many similarities. There are about 800 different "breeds" of sheep with many different physical characteristics. Depending on the breed, puberty occurs between 5 and 12 months. Breeding occurs throughout the year in domestic sheep and is somewhat dependent on photoperiods. The duration of estrus is in between 3 and 72 hrs. (average 29 hrs.); it is influenced by the presence of a male. The estrous cycle averages 16 days.
While the length of gestation in wild sheep species varies between 150 and 180 days, the domestic sheep has an average length of gestation of 148 days. Most sheep produce singletons, but some races regularly have twins, even triplets. Singletons weigh about 1.5 kg (Alexander, 1964). The placental weight is difficult to ascertain as the membranes are voluminous and of little importance to fetal growth as such. Kleemann et al. (2001) provided weights around 600 g. They were interested in the relation of placental and fetal sizes after progesterone treatment in early gestation. Whether these weights reflect a direct relation to the provision of nutrients to the fetus can be questioned. Therefore, investigators have weighed what they considered to be the most meaningful weight - that of blotted cotyledons. This is discussed below in detail (Alexander, 1964).
Within three to four days, the fertilized ovum reaches the uterus as a morula. The blastocyst develops by day 6 and sheds its zona pellucida by day 8 or 9. The blastocyst enlarges rapidly after the tenth day (Assheton, 1906). It becomes "sticky" and, on about day 17-18, it attaches with cytoplasmic protrusions to the endometrial surface. Naturally, this attachment is principally at the caruncles of the endometrium. The placenta remains diffuse for the first month or so after its mesometrial attachment (King et al., 1982). Lawn et al. (1969) did an electronmicroscopic study of goat and sheep placentas. Their youngest sheep gestation was at 42 days of pregnancy; the cotyledons were then just beginning to develop a villous structure. The trophoblast was apposed to an intact endometrium that had the appearance of protein secretion. Microvilli were abundant and occasional binucleated trophoblastic cells were present. Interdigitation of the cells progressed thereafter and the endometrial epithelium began to transform. Moreover, multinucleated giant cells became apparent. The syncytial cytoplasm then also acquires characteristic cytoplasmic granules.
|Uterine caruncles of immature common waterbuck (Kobus kob) with normal endometrium in between. (Courtesy, Dr. P. Hradecky).|
General characteristics of placenta
The sheep placenta is a polycotyledonary placenta with 70 to 100 cotyledons. Number and size of cotyledons varies widely with maternal age, strain of sheep and perhaps it depends on yet some other factors. The cotyledons are the fetal portions of the placentomes. The latter term, placentome, additionally encompasses the maternal caruncle.
In between the cotyledons is the intercotyledonary chorion, which has an additional and different absorptive function. It is covered by simple trophoblast and modified only over the mouths of endometrial glands. These regions are referred to as the "areolae". In between the areolae there are the "arcades" with focal hematomas and absorption of blood by trophoblast.
After the initial expansion of the blastocyst at about day 10, the elongated chorionic sac fills both of the uterine horns. It is entirely covered with trophoblast. This large sac contains a large, elongated allantoic cavity that apposes the chorion to the end of the outer chorionic sac and apposes the amnion directly over its central portions. The yolk sac is short-lived and plays no major role in ovine placentation and it cannot be found at term.
A bighorn sheep placenta received in May, 2004 weighed 300g, measured 83 cm in longest dimension, had 51 small concave cotyledons and a 27 cm long umbilical cord with four vessels.
|Diagram of opened sheep placenta. The largest compartment is the allantoic sac. Inside is the smaller amnionic cavity with the fetus. Dark spots are the placentomes - cotyledons.|
|Immature sheep placentome. The pale areas are villous tissue; in between villi are the maternal sheaths.|
(1987) differentiated between three types of cotyledons: the "flat"
kind of certain deer, the "convex" kind of other deer
and giraffes, and the "concave" kind of sheep and caprines.
The concave cotyledonary sheep placenta implants primarily upon the uterine
caruncles. In between the cotyledons, the chorion is simple and lacks
villi. The trophoblast intertwines with the uterine endometrium in the
caruncular regions, to form the so-called "placentome". Following
death of a pregnant animal it is easy to peel the placenta away from the
endometrium, without significant damage to either structure. There is
a large allantoic sac filled with urine. Urine is led to it through the
allantoic duct and that passes from the dome of the bladder through the
umbilical cord. Some urine must also pass through the urethra into the
amnionic cavity. Sheep possess multiply branched villi, in contrast to
some other ruminants. In reconstructions they appear as folds, rather
than the multiply branched thin villi that are seen in primate placentas.
|Immature sheep placenta with loosely constructed villi and thin region of maternal tissue, "plates".|
|Immature sheep placenta with loosely constructed villi and thin region of maternal tissue, "plates".|
|Implantation site of immature sheep placenta. Note the pink maternal tissue tongues with blood vessels penetrate between the villi.|
|Branching villus with trophoblast cover (T) adjoining the maternal epithelium.|
|Branching fetal villus with fetal blood vessel covered by trophoblast (see binucleate cell at right). The maternal epithelium seems to be focally broken.|
|Mature villous tissue with binucleate cells at arrowheads. The maternal tissue is adjacent but very difficult to identify. Many giant cells.|
For many years, the nature and origin of these giant cells has been disputed in the literature. Wimsatt (1950) considered them to be trophoblastic in origin. A later electronmicroscopic study by Davis and Wimsatt (1966) reaffirmed the trophoblast derivation of the syncytial (giant) cells. These authors then suggested movement of binucleate cells into the crypts where the giant cells develop. Wooding (1983) stated that the binucleate cells comprise as many as 1/5th of the trophoblastic population of ruminant placentomes. Another 1/5th of the binucleate cells was "migrating" and, in sheep, they were closer to the maternal tissues than the remainder of trophoblast. They arose early in gestation and decreased significantly towards term. A syncytium with uterine epithelium develops it is later replaced by cellular endometrial epithelium. One or two mitoses per 100 cells are present in the trophectoderm, but none in the syncytial giant cells.
Lee et al. (1986) studied binucleate cells with an antibody (SBU-3) that was found to interact commonly with most ruminants (deer, sheep, and cow). Binucleate cell cytoplasm stained with this antibody, both in the placentomes and in the intercotyledonary regions. These investigators, however, did not find this immunological marker to be expressed in the syncytial giant cells. This has to make one reconsider the true origin and nature of the syncytial giant cells. I believe that their origin from trophoblastic binucleate cells is not totally verified. Additional studies are needed.
Another area of special study by Wimsatt (1950) was the subchorial hematoma and pigmentation. At the top of the villous tree (and to a lesser extent in the "arcades" of the intercotyledonary membrane) significant amounts of maternal blood extravasate. The liberated red cells are here lysed and phagocytosed by trophoblast. As a result, large quantities of yellow ("nonferruginous") pigment accumulate. These hematomas are well developed in late pregnancy, and bleeding may occur intermittently throughout gestation. The precise vascular location of the origin of these hemorrhages is also uncertain. The blood may derive from peripheral capillaries of the septal tips in which Wimsatt observed degenerative changes. Others have suggested that the hematomas are the result of trophoblastic invasion which is, however, less evident at these sites than elsewhere in the cotyledons.
|Surface of cotyledon with large maternal hematoma and adjacent pigment-laden trophoblast (mouflon).|
|Surface of placenta with massive pigment accumulation in trophoblast. This is derived from former maternal hemorrhages.|
The umbilical cord attaches mesometrially. It has four large allantoic blood vessels (2A, 2V) and a large, patent allantoic duct. In addition to the four large blood vessels, there are numerous smaller allantoic vessels. They are especially congregated around the large allantoic duct. The cord of one bighorn sheep measured 27 cm in length and had no spirals.
The surface of the umbilical cord has numerous plaques (verrucae) that are composed of foci of squamous metaplasia with much keratin. There are few descriptions of the length of the ovine umbilical cord. Arvy & Pillery (1976) gave the length of ovine cords as being 7 cm, while Reynolds (1952) found it to be 10 cm. The umbilical cord of the sheep has no spirals. Reynolds studied the compression of Wharton's jelly by forcefully injecting the cord vessels and found that Wharton's jelly was only slightly compressible in sheep and goats, much less so than was found for human cords.
|The umbilical cord surface has many plaques of squamous metaplasia (verrucae), next to its thin amnionic epithelium.|
|Diagram of the intercotyledonary membranes attached to the uterus.|
|"Internal" membranes of sheep placenta with the amnion above. Beneath it is the allantoic membrane. Note that it is the allantoic chorion that contains the blood vessels. The amnionic connective tissue is avascular.|
are no "free" membranes in the sheep placenta. Between the cotyledons,
however, the intercotyledonary chorion is located, which is a relatively
simple membrane. It is avillous and covered on the outside with a simple
layer of cylindrical trophoblastic epithelium that has a microvillous
surface. The trophoblastic epithelial cells have a varied morphology,
as is evident in the next photograph. They are pressed against the endometrium
by pressure from within the allantoic cavity. In late stages, the exocoelomic
space is completely obliterated. The allantoic sac, which is of endodermal
origin, fuses with the chorionic sac as early as on the 22nd day of development
(Davies & Wimsatt, 1962). It is very large and elongate. Its columnar
epithelium possesses only very short microvilli and, in the mature placenta,
it is relatively flat. Davies (1952) was perhaps the first to draw attention
to the accumulation of large amounts of fructose in the allantoic fluid.
of the intercotyledonary membranes. The trophoblast below is apposed to
the uterine epithelium. It has a microvillous surface. This membrane lies
outside the allantoic sac, which is shown above. The allantoic sac has a
thick epithelial lining that is of endodermal origin, but it has only very
short microvilli. Both membranes have a vasculature.
Trophoblastic lining of the outside of the intercotyledonary membrane with pronounced microvillous surface. Note the pleomorphism of epithelial cells.
structure of the ovine amnion has been studied by Bautzmann & Schroder
(1955). Their investigations of the amnion from birds and reptiles had disclosed
the presence of a smooth musculature in the amnion. This is absent in sheep
and other mammals. The ovine amnionic epithelium is flat and single-layered,
with occasional "warts" or verrucae. They are composed of squamous
proliferations and are similar to the verrucae of squamous metaplasia in
the amnionic epithelium of the umbilical cord. These authors described in
detail also the collagenous fibers and the glassy membrane of the amnion.
These layers were further delineated in the detailed studies of human placental
membranes by Bourne (1962). Additional studies on these epithelial proliferations
in hoofed animals and whales were published by Naaktgeboren & Zwillenberg
(1961). They found them in essentially all hoofed animals and whales with
the exception of the pig. In sheep, they were initially white but became
yellow as gestation advanced. The allantoic sac also contains irregular
quantities of brownish debris, the hippomanes.
Trophoblast external to barrier
Numerous studies have addressed the hormonal output of the binucleate trophoblastic cells. Thus, Wooding et al. (1986) showed that 15-20 % of trophoblast are binucleated and contain ovine placental lactogen. Their number decreases shortly before parturition but this decline was prevented by fetal hypophysectomy, indicating fetal control of this population of cells. That this is due to fetal cortisol levels was elegantly shown in their subsequent experiments (Ward et al., 2002) which indicated an inverse correlation of cortisol levels and binucleate cell numbers. Nevertheless, even at very high levels of cortisol, a small number of binucleate cells remained. Miyazaki et al. (2002) studied the development of caprine trophoblast and binucleate cells by in vitro manipulation of a caprine trophoblast cell line.
|Sheep brain with spongiform encephalopathy.|
Sheep and goats commonly harbor Chlamydia psittaci organisms in their generative tracts. This infection often leads to abortion or birth of weak lambs. In subsequent pregnancies, the infection recurs in some 5-10%, with some immunity resulting (Wilsmore et al., 1990). In addition, vaginal shedding of organisms occurs. The placenta contains numerous organisms, and areas of inflammation and necrosis are found. Pregnant women attending delivery of infected ewes have repeatedly developed severe febrile illnesses, aborted and developed placental lesions characteristic of this infection (Hyde & Benirschke, 1997).
of intrauterine infection (psittacosis) by a human fetus of a farmer's wife
who helped with lamming in an infected sheep colony. Chorionic vascular
FV= fetal vessel; IVS=intervillous space.
|Placenta of intrauterine infection (psittacosis) by a human fetus of a farmer's wife who helped with lamming in an infected sheep colony. Infected syncytium with antibody staining. IVS=intervillous space.|
infectious diseases affect sheep. They have been summarized in the veterinary
literature, e.g. by Smith et al. (1972). Among these is brucellosis due
to infection with Brucella ovis. It causes mainly epididymitis in
rams but may affect the female generative tract and lead to abortion with
Most of the animal photographs in these chapters come from the Zoological Society of San Diego. I appreciate also very much the help of the pathologists at the San Diego Zoo.
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