Comparative Placentation

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Pygmy chimpanzee
Pan paniscus

Order: Primates
Family: Pongidae

1) General zoological data of species
[With notes on the common chimpanzee]

This smaller of the two chimpanzee species has been the topic of many studies, most comprehensively that of de Waal (1997). Bonobos, the common term used for this species, originate from central Zaire. They were described first and separated from other chimpanzees in 1933 by Coolidge. The species is now severely endangered and captive animals are managed by a Species Specialists Plan that publishes periodic action plans. The animals live in groups of up to 40, but usually much smaller groups are found. Life span is beyond 50 years. There are around 130 bonobos in various zoological gardens. They are listed by de Waal (1997). The status of bonobos in captivity was also reviewed by Benirschke et al. (1980). This smaller of the two Pan species has usually only one newborn. Several contributions with respect to the taxonomic origin of the pygmy chimpanzee and the dispute over the number of common chimpanzee species/subspecies can be found in the first volume "The Chimpanzee", edited by G. Bourne (1969). It also contains the skeletal anatomy, cerebral anatomy and some infections of chimpanzees.

		Group of pygmy chimpanzees of San Diego Zoo's Pan paniscus colony.

2) General gestational data

Gestation is around 230 days, and newborns weigh around 1.5 kg. The animals breed throughout the year and have a birth interval of 3 or more years. Single young are the rule, twins are exceptional. The young is usually born after a gestational period of about 220-230 days. Male adults weigh on average 43 kg, females are 37 kg. The placental weight at term, formalin-fixed, was 185 g without cord and membranes. Newborns weigh between 1,060 and 1,620 g (Puschmann, 1989). Another term placenta weighed only 68 g (?complete) and had a 73 cm long umbilical cord; its surviving neonate weighed 1,300 g.

		Typical facies of Pan paniscus.

3) Implantation

The implantation of the blastocyst is essentially the same as in humans. It occurs at a mid-uterine location, is invasive and is accomplished with penetrating trophoblast. The relation is hemochorial. The placenta is similar also to the common chimpanzee (Pan troglodytes). For that reason that species will not be separately considered but some specific data on common chimpanzees are appended at the end of this chapter.

		The umbilical cord of bonobos is characteristically long.

4) General characteristics of placenta

The bonobo placenta has great similarity to the human placenta, except for the apparently longer umbilical cord and its commonly marginal insertion. It is ovoid or round, has cotyledonary subdivisions and its general appearance is exactly like human placentas. It is smaller, as are the newborns and adults. The size of a term placenta was 15 x 8 x 3 cm. Another placenta was 13.5 x 9 x 1 cm. The histologic appearance is also much like that of human placentas, including X-cell cysts. The barrier is typical hemochorial. Macroscopically, the placenta is round or ovoid. There is invasive trophoblast that penetrates the decidua basalis.

		Villi of mature bonobo placenta.

		Placental floor with extravillous trophoblast infiltrating the decidua basalis at left.

		Detail of several terminal villi of mature bonobo placenta.

5) Details of barrier structure

This is a characteristic hemochorial placenta, much similar to that of human placentation. Villi do not anastomose, are covered by syncytium and, at term, the cytotrophoblast (Langhans' cells) are invisible in paraffin sections. They can be demonstrated by EM.

6) Umbilical cord

There are two arteries and one vein, no additional ducts. The cord is long, at least 76 cm (the most recent specimen) and 0.4 cm in diameter. It has few twists and little Wharton's jelly. The other specimen's umbilical cord that I was able to examine was 73 cm in length. As is true for most gorilla placentas, the cords were marginally inserted.

7) Uteroplacental circulation

No studies have been reported.

8) Extraplacental membranes

There is typical decidua capsularis as in other apes, with the chorion laeve showing atrophied villi. There is no allantoic cavity at term.

9) Trophoblast external to barrier

The extravillous trophoblast shows slight superficial invasion into the myometrium.

10) Endometrium

The endometrium undergoes decidualization much like that which occurs in human uteri. Menstrual bleeding occurs, as in humans, and lasts 3-4 days.

11) Various features

There is no subplacenta. The most remarkable feature of chimpanzee placentas when compared to human placentas is the length of the umbilical cord.

12) Endocrinology

In most cases, the placenta is eaten by the mother and direct analyses of placental hormones have not been done. Total estrogen levels during pregnancy are lower than in humans, but higher than in gorilla pregnancies.

As in gorilla and other apes, chorionic gonadotropin is found throughout pregnancy. The syncytiotrophoblast produces corticotropin-releasing hormone (CRH) and the pregnant serum contains its binding protein, CHR-BP (Bowman et al., 2001).

Czekala et al. (1981) compared immunoreactive estrogen of a variety of primates, including that of the bonobo and found them to be much lower than in human and orang utan gestations. Measurements of LH were not specific and included chorionic gonadotropin. The authors concluded, however, that the determinations are sensitive enough to diagnose pregnancy and thus enable pregnancy monitoring.

An extensive study of hormones (urinary and fecal) was undertaken by Jurke et al. (2000). They found abundant conjugated progestin and estrogen metabolites in urinary samples, while only traces existed in feces. Cortisol measurements indicated that they may be useful to gauge "stress".

13) Genetics

Bonobos have 48 chromosomes with great similarity to those of common chimpanzees and humans (Benirschke et al., 1974; 1985; Khudr et al., 1973; Bogart & Benirschke, 1977a,b). Jones et al. (1995) considered the relation of bonobos in evolutionary terms to other apes and man, a discussion that is still ongoing today. Banding patterns have been employed for paternity diagnosis (Benirschke & Kumamoto, 1985).

Hybrids have not been reported. We have observed a neonatal death due to trisomy 18, as proven with FISH staining of interphase cells. The clinodactly, cardiac interventricular septal defect, and ear anomalies found in this neonate were similar to those seen in human trisomy 18 (please see the last pictures). There was also significant lordosis and retarded growth (1,200 g, 21.8 cm CR length, brain weight of 122 g) (See Lear et al., 2001).

An important mutation (human CMP-sialic acid hydroxylase) has been described as having occurred at the Homo-Pan divergence (Chou et al., 1998).

14) Immunology

The blood group A antigen of bonobos and chimpanzees are the same as those of humans. Many other aspects of immunological relations to other apes and man are detailed in Jones et al. (1995).

15) Pathological features

Abortions have occasionally been observed, including a trisomy 18 neonate, similar to that of humans (Lear et al., 2001). Occasional spontaneous abortions occur in both species but for reasons not fully investigated; perhaps trisomies occur more often in bonobos, as they are common in human gestations. Thus, trisomy 22 has been seen at birth (Benirschke et al., 1974). This is, genetically speaking, identical to human trisomy 21. Scott (1992) described cardiac hypertrophy perhaps resulting from cardiovascular disease in a 21-year-old male animal. We have seen a dissecting aneurysm of the aorta as the cause of death in a male bonobo.

Lasley et al. (1977) described reproductive failure from former gunshot wounds and with consequent ovarian dysfunction. Smith et al. (1983) identified calicivirus persistence in the bonobo. Ascending intrauterine infection (chorioamnionitis) with funisitis and premature birth has been seen in common chimpanzee.

		Umbilical phlebitis - numerous polymorphonuclear leukocytes are emigrating to the cord's surface.

16) Physiological data

No publications are known to me.

17) Other resources

Fibroblast strains are available through CRES at the San Diego Zoo.
Pregnancy and birth of a common chimpanzee following artificial insemination with post mortem frozen epididymal sperm has been reported by Kusunoki et al. (2001).

References

CRES at: http://www.sandiegozoo.org/conservation/cres_home.html

Benirschke, K. and Kumamoto, A.T.: Paternity diagnosis in pygmy chimpanzees. Intern. Zoo Ybk. 23:220-223, 1985.

Benirschke, K., Bogart, M.H., McClure, H.K. and Nelson-Rees, W.A.: Fluorescence of the trisomic chimpanzee chromosomes. J. Med. Primatol. 3:311-314, 1974.

Benirschke, K., Bogart, M.H. and Adams, F.: The status of the pygmy chimpanzee. Intern. Zoo Ybk. 20:71-76, 1980.

Bourne, G.H., ed. The Chimpanzee, Vol. 1: Anatomy, Behavior, and Diseases of Chimpanzees. University Park Press, Baltimore, 1969. (and Karger, Basel).

Bogart, M.H. and Benirschke, K.: Chromosomal analysis of the pygmy chimpanzee (Pan paniscus) with a comparison to man. Folia Primatol. 27:60-67, 1977a.

Bogart, M.H. and Benirschke, K.: Q-band polymorphism in a family of pygmy chimpanzee (Pan paniscus). J. Med. Primatol. 6:172-175, 1977b.

Bowman, M.E., Lopata, A., Jaffe, R.B., Golos, T.G., Wickings, J. and Smith, R.: Corticotropin-releasing hormone-binding protein in primates. Amer. J. Primatol. 53:123-130, 2001.

Chou, H.-H., Takematsu, H., Diaz, S., Iber, J., Nickerson, E., Wright, K.L., Muchmore, E.A., Nelson, D.L., Warren, S.T. and Varki, A.: A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc. Natl. Acad. Sci. 95:11751-11756, 1998.

Coolidge, H.J.: Pan paniscus (Pygmy chimpanzee) from south of the Congo River. Amer. J. Phys. Anthropol. 8:1-57, 1933.

Czekala, N.M., Hodges, J.K. and Lasley, B.L.: Pregnancy monitoring in diverse primate species by estrogen and bioactive luteinizing hormone determinations in small volumes of urine. J. Med. Primatol. 10:1-15, 1981.

de Waal, F. and Lanting, F.: Bonobo. The Forgotten Ape. University of California Press, Berkeley, 1997.

Jones, S., Martin, R. and Pilbeam, D., eds.: The Cambridge Encyclopedia of Human Evolution. Cambridge University Press, Cambridge 1995.

Jurke, M.H., Hagey, L.R., Jurke, S. and Czekala, N.M.: Monitoring hormones in urine and feces of captive bonobos (Pan paniscus). Primates 41:311-319, 2000.

Khudr, G., Benirschke, K. and Sedgwick, C.J.: Man and Pan paniscus: A karyologic comparison. J. Human Evol. 2:323-331,1973.

Kusunoki, H., Daimaru, H., Minami, S., Nishimoto, S., Yamane, K.-I. and Fukumoto, Y.: Birth of a chimpanzee (Pan troglodytes) after artificial insemination with cryopreserved epididymal spermatozoa collected postmortem. Zoo Biol. 20:135-143, 2001.

Lasley, B.L., Kennedy, J.F., Robinson, P.T., Bogart, M.H. and Benirschke, K.: A study of reproductive failure in a pygmy chimpanzee (Pan paniscus). Zool. Garten 47:289-295, 1977.

Lear, T.L., Houck, M.L., Zhang, Y.W., Debnar, L.A., Sutherland-Smith, M.R., Young, L., Jones, K.L., and Benirschke, K.: Trisomy 17 in a bonobo (Pan paniscus) and deletion of 3q in a lowland gorilla (Gorilla gorilla gorilla): comparison with human trisomy 18 and human deletion 4q syndrome. Cytogenet. Cell Genet. 95:228-233, 2001).

Puschmann, W.: Zootierhaltung. Vol. 2, Säugetiere. VEB Deutscher Landwirtschaftsverlag, Berlin, 1989.

Scott, G.B.D.: Comparative Primate Pathology. Oxford University Press, Oxford, 1992.

Smith, A., Skilling, D.E., Ensley, P.K., Benirschke, K. and Lester, T.L.: Calicivirus isolation and persistence in a pygmy chimpanzee (Pan paniscus). Science 221:79-81, 1983.

Additional consideration of the placentation in the common chimpanzee,
Pan troglodytes

Several placentas have become available to us that differ only in minor detail from that of the bonobo. Thus, the term placenta of one such animal was 300 g, had an eccentric umbilical cord insertion, but the cord was only 26 cm long. It had a chalky streak, which was interpreted as being a calcified vitelline duct remnant. The remainder was normal.
Another placenta had typical "X-cell" cysts (extravillous trophoblast). One additional placenta was of fraternal twins (male/female). It was kindly made available by Mrs. Jo Fritz (Arizona). It was from a premature delivery and was an example of a fused diamnionic dichorionic twin placenta, weighing 230 g combined. One cord was 15 cm, the other 49 cm long and one had a right, the other a left twist; one was eccentric, the other was marginal in its insertion. One had funisitis, a common cause of premature birth in human pregnancies. An unexplained feature of this specimen was the large number of hemosiderin-laden macrophages in the villi of twin 2.

		Twin placenta of common chimpanzee, a fused, diamnionic, dichorionic organ.

		Umbilical cord of common chimpanzee calcific streak

		Facies of neonatal bonobo with trisomy 18 born at the San Diego Zoo who died neonatally.

		Facies of neonatal bonobo with trisomy 18 born at the San Diego Zoo who died neonatally.

		Facies of neonatal bonobo with trisomy 18 born at the San Diego Zoo who died neonatally.

contact me: kbenirsc@ucsd.edu