Equus caballus by
Manu Sebastian, Lexington, KY
Kurt Benirschke, San Diego, CA
General Gestational Data
General Characterization of the Placenta
Details of fetal/maternal barrier
The surface of microcotyledons and their villous branches is a single layer of uninuclear trophoblast. Binucleate cells, as seen in ungulate placentas, are absent there; they are seen only at the girdle. There is no invasion of maternal tissue, rather, the trophoblast directly abuts the endometrial epithelium in a complex manner in the villous portions of the placenta. As pregnancy proceeds, the proximity of this exchange area increases and there is then a very close approximation of fetal and maternal capillaries. Only beneath the chorionic surface is the trophoblast more cylindrical and often vacuolated. Here also, some yellow pigmentary inclusions are found. They are iron-stain negative and may, as in ungulates, represent melanin, but other pigments cannot be excluded. We have not found this pigment further discussed in the equine literature except to note that, generally, it is assumed that iron is transported to the fetus with uteroferrin from endometrial secretions (Wooding et al., 2000). This cylindrical structure of the trophoblast is also apparent in between the microcotyledons, the areolae or arcades. It is assumed to have a histotrophic function for absorption of uterine secretions.
There is considerable variation in the finer structure and size of microcotyledons that has been assessed quantitatively by Wilsher & Allen (2003). Their extensive data show convincingly that there is a strong correlation of villous surface and fetal weight; primiparous mares (especially older primipara) had smaller foals, in part or perhaps wholly because of this smaller villous surface area. Various other quantitative data are given in this excellent contribution.
Jones et al. (2000) examined the pattern of glycosylation of the "interhemal barriers" of horse, donkey, and camel. This was similar between horse and donkey but much different in the camel. From this it was suggested that this may be important to prevent interspecific hybrids. Macdonald et al. (2000) studied the villous structures of the horse by scanning electron microscopy and published impressive, conclusive pictures of maternal and fetal aspects of the pony placentas. This suggested to them that the "microcotyledons" are the aggregates of encapsulation of 16 uterine crypt regions. With advancing gestation the villi kept branching until very close to term.
The umbilical cord of horses has been described in considerable detail by Whitwell (1975). It has a somewhat longer portion within the amnionic cavity and a shorter segment in the allantoic sac; but that varies. The membrane insertion delineates these two segments. There is a considerable variability in the length of the cord, with measurements from 36 to 84 cm in the thoroughbred foals (mean 55 cm) of her study. Excessive lengths have been considered to be the cause of abortion, of fetal strangulation, and of fetal demise (Whitwell, 1975; Caslick, 1932, others). The ultimate cause for this variability in cord lengths is unknown. Caslick measured lengths from 30.5 to 137.2 cm, with the variability perhaps being more distributed over the amnionic portion.
The length of the umbilical cord is surely determined in early gestation, as abortions with excessive lengths occur not uncommonly. Also, in contrast to many other species, the horse fetus has great mobility in early gestation. Similar variations in length occur in human placentation; and short cords are usually due to lack of fetal motion (Benirschke, 1994; Snider, 1997). One wonders whether mobility is perhaps in part the result of the "breed" of horse and notes that the variability in length of the horse cord is often in the amnionic portion. One can imagine that race horses might be more mobile, perhaps already in utero, than draught horses. Measurements comparing different "breeds" are outstanding but would be of great interest.
There is often considerable twisting of the horse umbilical cord. It has occasionally led to excessive torsion and strangulation, with impressions left on the stillborn foal (Whitwell, 1975; Hong et al.; Giles et al., 1993). Perhaps it is also the cause of some of the allantoic duct dilatations (6%) observed by Whitwell & Jeffcott (1975).
The latter authors found the cord to be inserted at the posterior aspect of the uterus, either in or near midline, or in the pregnant horn. The umbilical cord contains two arteries and one vein, in addition to a widely patent, thin-walled allantoic duct. It is accompanied by strands of smooth muscle fibers. While two major venous branches expand over the allantochorion, they fuse to become a single vein at the passing through the amnionic insertion around the cord. The allantoic portion of the umbilical cord is not a solid cord but a "web of vessels" (Whitwell, 1975). In addition to the three large vessels, numerous smaller blood vessels are also present in the umbilical cord, especially in the vicinity of the allantoic duct. Remnants of the vitelline duct may be present and Whitwell has identified remnants of the yolk sac in all placentas she has studied (personal communication). The cord may be significantly spiraled and, in the amnionic portion, it has many very small foci of sqamous metaplasia on its surface.
Absence of one umbilical artery was seen once in 145 cords with a fetus having renal anomalies. Furthermore, in excessively long umbilical cords and heavily spiraled ones, thrombosis and vascular calcification have been observed. The last kiang placenta observed had four umbilical vessels and no twists at all.
Steven (1982) showed an excellent diagram of the vasculature in the uterus that supplies the microcotyledons and the arcades. It has been repeated in many subsequent publications on the horse placenta. He depicted the straight maternal arteries to proceed between the microcotyledons whose branches then enter the endometrium that correspond to the microcotyledons. The veins draining this tissue pursue a central flow from the centers of the microcotyledons. Moreover, towards term, there is more and more "invagination or infiltration" of the fetal capillaries into the trophoblast so that, at the end of gestation, fetal and maternal capillaries come to lie in very close physical proximity. This assures maximal possibility of nutrient/gaseous exchange.
amnionic epithelium is a thin, single layer of cells with frequent areas
of squamous metaplasia ("pustules, plaques") whose cells contain
The hippomanes are yellowish/green pasty concentration products of fetal urine and contain large numbers of birefringent crystals (some of which are oxalates). The material is acellular and probably mostly composed of these crystals, protein and urinary detritus cells. The last kiang placenta was accompanied by one large 35 g flattened piece of hippomanes.
Equines have an initially large yolk sac that remains functional for a month and then regresses completely, leaving a tiny remnant in the cord insertion.
Trophoblast external to barrier
The only "invasion" of uterine tissue occurs at the chorionic girdle with the development of temporary "endometrial cups". There is an intense inflammatory response, probably because of this infiltration. This is further discussed above and also in the section on immunology.
recently, relaxin has been localized to the horse placenta (Klonisch et
al., 1995). While it had been known for some time that relaxin was produced
by the equine placenta, this is the first report to localize it to trophoblast
and to establish an assay. The serum quantity shows marked differences among
horse breeds and declines after parturition. Recent studies have suggested
that the decline in serum relaxin levels may be useful for the prediction
of placental problems (infection, impending abortion, and the like) and
that corrective therapy (e.g. antimicrobials) may be administered to rescue
the pregnancy (Ryan et al., 1999).
other genetic studies have been conducted in horses. Especially blood groups
and serum proteins have been studied to assess the genetic variety and breadth
of populations. This literature can be accessed from the paper by Cothran
et al. (1998) who studied the polymorphism of the "Pantaneiro"
horse of the Brazilian Pantanal. Despite a presumably small original stock,
an ordinary degree of polymorphism was found and this is compared with many
other breeds of horses.
|It is occasionally possible to absolutely prove the occurrence of maternal septicemia as the cause of fetal infection. This was for instance the case in the example of congenital coccidioidomycosis shown next. This infection has been a particular problem in San Diego where a number of Przewalski's horses have been lost to this fungal infection. The dry soils of this region and Arizona contain this organism commonly.|
addition to these reasons for abortion, an excessively long umbilical
cord often caused fetal demise by "strangulation". This has
been alluded to in the discussion on umbilical cord above and is also
the topic of the publications by Vandeplassche & Lauwers (1986), and
that by Hong et al. (1993). The latter authors found the normal cord length
to be 52 cm; 4.5% of 1,211 abortion cases were due to excessively long
cords with torsion and they were 72 cm long. The large survey of abortions
and stillbirths by Smith et al. (2003) makes the same observations. What
remains to be elucidated is why this is so relatively common in horses,
as compared to its rare occurrence in most other species.
In addition to the acardiac twin, we have described a placental teratoma (Gurfield & Benirschke, 2003). Interestingly, the mare remained well later, thus precluding metastases from an ovarian teratoma. Most of the tissue had the appearance of dysgerminoma, but more mature elements (skin, thyroid, cartilage, etc.) were also found. It may therefore be of additional interest that we have identified two cases of benign cystic teratoma in the membranes of kiang placentas (see chapter on Kiang). Since that publication, another placental teratocarcinoma with possible metastases to the foal was described by Allison et al. (2004). The foal died in 2½ months from metastases.
Griner (1983) summarized a variety of pathologic features that he identified in exotic equidae of the San Diego Zoo. Trauma, neonatal deaths from omphalitis and intestinal helminths were the principal reasons for mortality. The next pictures are from a "papillary region" in the surface of the placenta that was initially interpreted as being squamous metaplasia. Higher magnification shows no desmosomes and the hypertrophied cells are continuous with the villous trophoblast. We have seen only one such lesion and believe that it represents a benign proliferation of trophoblast.
|Several investigators have described this "adenomatous hyperplasia" (dysplasia) of the equine allantois. (McEntee et al., 1988; Hong et al., 1993; Shivaprasad et al., 1994). It takes the form of numerous nodules on the allantoic membrane surface and is composed of glandular structures (that may contain secretions) embedded in loose connective tissue. Occasionally it is associated with neutrophilic infiltration but an infectious etiology probably does not always exist. McEntee et al. (1988) believed the lesion to be "dysplastic" and could not correlate it with abnormal fetal or neonatal growth. In contrast, however, Shivaprasad et al. (1994) found it to be correlated with abortion and fetal/placental infections. Grossly, the lesion appears as is shown in the next photographs, but it may also be even much more extensive.|
discharge in horses is conventionally referred to as "fetal diarrhea"
A typical case is shown in the next photograph. It is not altogether clear
to us whether the condition is similar to that observed in human gestations.
Meconium discharge in humans is common (+/- 15%) and is usually the result
of being post-dates (i.e. >40 weeks gestation). There is good reason
to believe that this results from the elevated levels of fetal motilin concentration,
rather than being secondary to "stress" (Benirschke, 2001). No
such studies have been undertaken in horses.
The next lesion of a horse placenta was sent to me by Dr. Berrington of Langley, British Columbia. The foal was normal and survived; the lesions come from the lesser horn and were described as "abundant, scattered fatty masses" attached to the maternal surface. Despite the vast experience of the breeder and pathologist, such lesions had never been seen and the question was raised whether this may be the equivalent of molar degeneration of human placentas. A few of the lesions were quite large and grape-like. In my opinion the lesions are more like what in human pathology we refer to as "chorangiomatosis", a proliferation of fetal villus capillaries and occurring in chronic hypoxic conditions as well as for no apparent reason.
Cowell & Tyler (2001) provided a detailed review of the hematology and cytology of numerous fluids and tissues. The relationship of fetal size to maternal size and the "supply line" has been examined several times, but most decisively by Allen et al. (2002a). They found that ponies had a 325 day gestation, while the thoroughbreds had a length of 339 days. To further understand the finer reproductive regulations, embryo transfer experiments were conducted. These were also designed to verify the original observations by Walton & Hammond of crossbreeding Shire horse with Shetland ponies (1938; see above). When embryo transfers were performed between these two breeds then the gestational length was intermediate, as were the foals' weights. The ponies in thoroughbred mares were significantly heavier and correlated with weights of mare and placental sizes. Moreover, the density of microcotyledons was greater in the thoroughbreds, irrespective of the foal they carried. Thus, the placental contact area, rather than genetic background of the horses is important. Endocrine findings were more complex (Allen et al., 2002b, see section 12 above).
Wooding & Morgan (1988) defined the sites for calcium and glucose exchange in the areolar regions of the placenta. In subsequent studies, Wooding et al. (2000) showed iron transport to be achieved by the uteroferrin, a protein secreted by the endometrium in response to progesterone (Groothuis et al., 1997). Its presence can be identified in the microvesicular transport system, different from the facilitated transport of calcium. This protein, as well as many other components of uterine secretions at various cycle days were better defined by Zavy et al. (1982).
Ridderstrale et al. (1997) studied the presence of carbonic anhydrase at the interface in a variety of species. There was relatively little activity in horse placentas.
Other remarks - What additional Information is needed?
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