Comparative Placentation

Lowland Gorilla
Gorilla gorilla

Order: Primates
Family: Pongidae

1) General Zoological Data

Lowland gorillas are an African species. There are local differences in phenotype and genetic makeup that subdivide Eastern and Western gorillas into subspecies, with perhaps additional subspecies. The larger Mountain gorilla placenta has not been studied and none of this endangered species are in captivity. Numerous gorillas have bred in captivity, in various zoos (Cousins, 1976). The largest colony exists in Aspinall's Howletts and Port Lympne Parks, Kent, UK (Aspinall, 1982). In Africa, the principal predator of gorillas is the leopard. Osteomyelitis from such an apparent attack has been reported by Tutin & Benirschke (1991).

		Typical term gorilla placenta, maternal surface at left. Note the long umbilical cord with few twists. Note also the circummarginate insertion of the membranes on the right.

2) General Gestational Data

Adult females weigh from 70-140 kg (Nowak & Paradiso, 1983). Newborns weigh around 2 kg and have closed skull sutures with thick skull bones. The estrous cycle is 31 days; usually one young is born after 251-295 days of gestation. Twins are uncommon and are usually stillborn or aborted (Rosen, 1972). The newborn weight is about 1.6 to 2 kg at term. Sexual maturity of females is reached at 8 years, and at 11 years in males. In captivity, the lifespan is over 50 years. The placental weight, at term (excluding membranes and cord), is around 350 g. The average placental disk measures approximately 15 x 13 x 2 cm. The membranes (chorion laeve) attach marginally or in a circummarginate fashion. The organ bears great similarity to human placentas, except for its smaller size and the longer umbilical cord. The most recently studied placenta from the "Safari Center" at San Diego Zoo Global was 15 cm in diameter and weighed 225 g. It had the cord knot to be described below.

Wislocki (1932) has described the anatomy and histology of the female reproductive tract, including placentation, in great detail.

		Gorilla group at the Wild Animal Park of the Zoological Society of San Diego.

		Mother and neonate gorilla at San Diego's Wild Animal Park.

3) Implantation

As is true of the human placenta, the gorilla placenta implants "interstitially", with decidua surrounding the entire implanted blastocyst. Once the membranes "herniate" into the uterine cavity, the peripheral villi, those on the membrane surface, atrophy. Implantation of the blastocyst onto the other endometrial surface does not occur. Thus, a single discoid organ forms with membranes like those in humans. The placenta is anterior or posterior in its location. A wide margin of membranes separates it from the endocervical canal.

4) General Characterization of the Placenta

Other than for their smaller size, the discoid shape and appearance of the gorilla placenta are very similar to those of human placentas. It is cotyledonary with few, relatively indistinct cotyledonary subdivisions seen on the maternal surface. There are much basal calcification and a considerable amount of fibrinoid material. The barrier is identical to that of humans, it is hemochorial and there is moderately extensive trophoblastic invasion of the endometrium and probably also invasion of the superficial myometrium. Vascular trophoblastic invasion occurs in the decidua basalis. There are large deposits of extravillous trophoblast ("X-cells") and some have cystic centers. The same cells infiltrate into the decidua basalis.

		Cyst of extravillous trophoblast ("X-cells")

		Term gorilla placental villus. It is much like the human.

	5) Details of fetal/maternal barrier The surface area of villous structures was determined by Baur (1970). It is similar to that of other ape placentas and humans. The surface is composed of syncytiotrophoblast with underlying cytotrophoblast. The syncytium has brush (microvillous) borders.

		Placental floor, villi below, much fibrinoid and mild calcification

		More term villi of gorilla placenta.

6) Umbilical cord

The umbilical cord of the gorilla placenta has two arteries and one vein. There are normally no ducts, but remnants of the former allantoic duct occasionally occur in between the two arteries. Compared to human umbilical cords (55 cm), that of the gorilla is unusually long, often as much as 100 cm. The reason for this extraordinary length is unknown. This aspect has been further discussed by Spatz (1968) who related the length of cords to fetal length. The most recently studied placenta had a 185 cm cord length with a true umbilical knot and the neonate did well.

The cord shown in our photograph was 70 cm long and there was an estimated 20 cm still attached to the newborn. The umbilical cord had apparently ruptured spontaneously or it was bitten through by the mother. This is not often observed in apes, nor is placentophagy, as was discussed by Naaktgeboren & Wagtendonk (1966). In our experience, the cord is most frequently marginally inserted in gorillas, but this was not so in the placentas shown here. Ludwig (1961a,b) also found a marginal insertion of a 65 cm long cord and in other umbilical cords that he observed. He considered the specimen depicted to be a "usual" gorilla cord, even though it had a true knot. The female offspring of this gestation did well.

	Last placenta seen with true knot and 185 cm long cord.

	This is the true knot in the cord.

	This is a section through the knot in the umbilical cord.

	Another section through the cord knot.

	Section through the cord away from the knot.

	The mother with offspring from the mother with long cord and knot.

	Remnant of allantoic duct in cord.

	7) Uteroplacental circulation This is essentially the same as in human gestations, except that the maternal decidual arterioles usually have thicker walls.

		Membranes with chorion at left and decidua at right. Note the thick, hyalinized arterioles.

	8) Extraplacental membranes Wislocki (1932) and others have shown the presence of a decidua capsularis with remnants of villi in the chorion laeve. The amnion is identical to the human placental amnion, and there is no allantoic membrane.

		Membranes with atrophied villus in between decidua (right) and chorion (left), within trophoblast layer.

9) Trophoblast external to barrier

There are extensive islands of "X-cells" and there is invasion by extravillous trophoblast into the decidua basalis and into the maternal vessels. Whether it also extends into the myometrium, as is true in humans, is unknown.

10) Endometrium

There is decidualization, much like that of human placentation with wandering trophoblast, which invades the decidua basalis.

11) Various features

In all respects this placenta is morphologically like human placentas.

12) Endocrinology

A complete review of hormones and their actions in primate pregnancies has been made by Pepe & Albrecht (1995). Much of this applies to gorilla pregnancies for which only few specific studies have been reported, e.g. Czekala et al. (1983), Watson (1984), Mitchell et al. (1982), and Martin et al. (1977).

Successful birth after embryo transfer was reported by Pope et al. (1997). These authors have provided much endocrine information as well and a comprehensive bibliography.

Chorionic gonadotropin is present during pregnancy, but the total urinary estrogen of gorilla pregnancies is significantly lower than that found in human or chimpanzee pregnancies. The syncytiotrophoblast of the ape placenta produces corticotropin-releasing hormone (CRH) and the serum of pregnant gorillas contains its binding protein (CRH-BP) (Bowman et al., 2001).

13) Genetics

Gorillas, as all large apes, possess 48 chromosomes with extensive homology to human chromosomes. Hybrids have not been described.

We have observed a growth-retarded, phenotypically normal 5 year-old gorilla that has a large deletion of chromosome 3 (at q30). The parents have normal chromosomes (Lear et al., 2001).

Mitochondrial DNA was used to differentiate among subspecies (Garner & Ryder, 1996); and Arnason et al. (1996) used mtDNA to survey patterns of hominid evolution.

DNA from hair samples has enabled paternity diagnosis (Field et al., 1998). Using FISH methodology for 24 specimens of gorilla, Schempp et al. (1998) localized human ribosomal DNA to chromosomes 22 and 23 (corresponding to 21 and 22 in humans).
The numerous publications on gorilla chromosomes and genetics are partially cited in the references below.

14) Immunology

No truly immunological studies of pregnancy are known to us.

15) Pathological features

Numerous reproductive diseases have been described, and a review of gorilla mortalities has been published (Benirschke & Adams, 1980). Examples include placental abruption with stillbirth and presumed preeclampsia equivalent to human gestations, fatally acute amebic meningoencephalomyelitis, tularemia, coccidioidomycosis, nephritis, ruptured aortic aneurysm, and a multitude of ailments similar to those found in humans. Scott (1992) and Griner (1983) have compiled some of this information in books. Other aspects of pathology are summarized in a book, which evolved from a primate meeting in 1985 (Benirschke, ed., 1986). Trophoblastic tumors and hydatidiform moles have not been described. Spontaneous abortions do occur, but their chromosomes have not been studied. Insufficient numbers of few placentas have been studied to eliminate ascending placental infections as a possible disease, as exists in chimpanzees.

In the placenta of abruptio and a few others we have observed, there occur typical infarcts, very similar to those seen in human placentas. Intervillous thromboses and so-called "Tenney Parker changes" (excessive syncytial knotting) also occur. Eclampsia, with a live-born neonate, was reported by Baird (1981); in my opinion, however, that diagnosis is somewhat dubious.

		Abruptio placentae with green and yellow discoloration at left; at right is the underlying infarct (From Benirschke, 1980).

		Term gorilla placental villi with focal necrosis and hemosiderin deposition in villus. The cause is unknown; in human placentas this would be suspicious of former hemorrhage or CMV infection.

16) Physiological data

Whereas alkaline phosphatase, (the most abundant enzyme of human placentas), is present in placentas of chimpanzees and orangutans, it is extremely low or absent in gorilla placentas (Doellgast et al., 1979, 1981). Information on blood groups and many other physiological data can be found in Benirschke, 1986.

Sonographic estimation of birth size has been advanced by Yeager et al. (1981).

17) Other resources

Cell strains of numerous gorillas and DNA are available from CRES at the Zoological Society of San Diego.

18) Other features of interest

Here follow a few examples of pathology with similarity to human reproductive pathology. Surely, many more of these conditions exist but that information is unpublished. One may ask, why are the umbilical cords of gorillas and chimpanzee twice as long as those of humans? What is the frequency of chromosomal errors at conception? Many comparative questions of this kind remain to be answered.

		Spontaneous abortus with hydatid villi lacking vessels and degenerating decidua. This is essentially similar to a human spontaneous abortus due to chromosomal error.

		This is another view of the aborted pregnancy. The villi are significantly enlarged (swollen, "hydatid"), but there is still a floor of decidua basalis. Villi contain no vessels and are comparable to what in human pregnancies might be a "partial mole" due to triploidy. No trophoblastic proliferation.

		Another, similar spontaneous abortus.

		A very young spontaneous abortus with defective embryo in the center of a blood-filled chorion.

		Infarct of mature placenta with live infant Decidual necrosis is on top.

		Histologic appearance of the infarcted placental tissue.

		Gorilla placenta with fetal vascular latex injection- note marginal cord and one-to-one correspondence of fetal blood vessels.

		Knot in umbilical cord of gorilla placenta, at right.

		Five year-old male gorilla with growth retardation, presumably due to a large deletion of a portion of one chromosome # 3.

		Stillborn gorilla male. Fetal death because of abruptio placentae.

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