Golden lion tamarin (Leontopithecus rosalia). | ||
Twin golden lion tamarin fetuses and placenta from Ryan et al., 1961. | ||
Uterus of pregnancy in previous figure before section. | ||
3) Implantation Implantation is antimesometrial with one lobe (placenta) anterior, the other posterior, but having extensive vascular connections. It is superficial and amnion forms by cavitation. Wislocki (1939) described occasional side-by-side implantation. The villous tissue is trabecular, without typical cotyledons. It is a hemochorial placenta and moderate decidua formation of the uterus simplex occurs. There is no allantoic sac. The remarkable features of marmoset and tamarin placentas are the inter-twin vascular connections between fraternal twins, and the villous hematopoiesis of the placentas. An early implantation has been described by Benirschke & Layton (1969). This case and two other early gestations described by Wislocki (1939) show the chorionic membranes to be fused prior to the development of fetal blood vessels. The exact time of implantation was unknown until the descriptions of Moore et al. (1985). They examined pregnant uteri from timed matings in Callithrix jacchus, the common marmoset and determined that implantation takes place around day 12 with invading syncytium. Later studies (Chambers & Hearn, 1985) examined the uterus every 10 days during pregnancy and provided an excellent guide of this species' placentation and fetal growth. Much of their work was done in thin sections and correlated with progesterone levels. Implantation appeared to occur over the mouth of an endometrial gland and was achieved by trophoblastic infiltration, rather than by such destruction as seen in other primates. Although some syncytial invasion into maternal vessels was observed (later, Smith et al., 1987, refuted this assumption in an electron microscopic study), most were free of trophoblast. There was early and marked trophoblastic proliferation, cytotrophoblast was very sparse but present. A detailed study of seven marmoset implantation sites between days 12 and 15 in Callithrix jacchus, accompanied by superb electronmicrographs was published by Enders & Lopata (1999). This paper also provides references to the endocrine means for precise timing of gestation in marmosets. This study confirmed the unusual growth of the early blastocyst/embryo that grows within the uterine lumen, rather than implanting deeply into the endometrium, as is the case in humans, for instance. This may relate to the delay of embryonic disk formation and the easier ability to culture their blastocysts. Fusion of syncytium with endometrial epithelial cells was observed. True invasion of the endometrium by the syncytiotrophoblast began on day 15. Cytotrophoblast always was the precursor of syncytium. In one of their cases the two blastocysts implanted on the same uterine surface, rather than on opposite sides as is the norm. The callithricid placenta contains maternal blood vessels, which were studied in detail by Merker et al. (1987). By day 48, the endometrial vessels around these vessels had disappeared and a prominent collagen-rich (types IV & V) layer (which also had laminin plus proteoglycan MB-1) developed, with gaps to allow perfusion. The basement membrane material appeared to have been produced by the endothelium. Electronmicroscopic studies were undertaken by several authors. Wynn et al. (1975) studied term placentas of two species and found a poorly developed decidual reaction, a "pseudolabyrinthine" (trabecular) organ, with an acellular junctional zone. The villous surface was similar to other primates with syncytium (endowed with much microvillous surface), and cytotrophoblast. There was little villous connective tissue. The "junctional zone" with the endometrium is relatively acellular with a small amount of Nitabuch fibrinoid and some mononuclear elements. Their study of amnion showed it is like that of other primates. They also described retention to term of a yolk sac, not seen by other students. Broad columns of trophoblast are rare. They do exist, however, in broad columns at early implantation. |
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Implantation
zone of tamarin placenta. Endometrium below (E = endometrial gland; F = Nitabuch fibrinoid; V = villi; C = broad sheets of cytotrophoblast anchoring the villi to endometrium). |
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Early twin blastocysts in golden lion tamarin (Benirschke & Layton, 1969). [E1 and E2 embryos, C=Chorion, A=amnion]. Note broad zone of invasion and large endometrial glands. | ||
Same as previous, actual photograph. | ||
Wall of large intraplacental maternal blood vessel with calcification and abundant basement membrane deposits. | ||
Fetal surface with amnion and fetal blood vessels. | ||
Complete cross section of tamarin placenta, amnion above. Note the trabecular structure. | ||
Higher power of tamarin villous tissue. Note clumped syncytium and focal villous hematopoiesis. | ||
Occasional singletons are born, like this pregnancy with a single placenta and no remnant of a twin. This is Saguinus oedipus. | ||
4) General characteristics of placenta The two disks (one for each twin) are monochorionic and usually closely approximated. Wislocki reported (1939) implantation of blastocysts in Saguinus geoffroyi to have occurred on opposite sides of the uterus or, in others, side-by-side. This author also reported on presomite embryos with early implantation and found equally early chorionic fusion. But the timing of this early implantation (or size/age of the embryos) was not stated. A detailed study of the hematopoiesis in placental trabeculae, first observed by Wislocki (1943), was provided by Jollie et al. (1975). They also gave fine-structural details. Hematopoiesis in the placenta occurred at all stages of gestation; it took place in the sinuses but it was primarily of the erythropoietic type.
5) Details of barrier structure |
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Higher power view of villous structures with fetal vessels, pronounced syncytial knots on villous surface. | ||
6) Umbilical cord There are three vessels in the umbilical cord and no ducts. The length of cords has been described by Spatz (1968) for pygmy and common marmosets as being 20-40 cm. It is eccentrically inserted and has few spirals. It is covered by thin amnionic epithelium. 7)
Uteroplacental circulation |
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Maternal floor of tamarin placenta showing large maternal vessel surrounded but not invaded by trophoblast. Areas of necrosis and Nitabuch fibrin layer are apparent. | ||
8) Extraplacental membranes Amnion is like that of other primates; there are in atrophied villi in the chorion laeve, but it contains bridging vessels. 9)
Trophoblast external to barrier 10)
Endometrium 11)
Various features 12)
Endocrinology 14)
Immunology
15) Pathological features |
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Term infant and macerated embryo with placenta of pygmy marmoset (Pygmaea cebuella). | ||
Occasional triplets occur, here one with maceration (right), but not with a separate placenta, Saguinus labiatus. | ||
Spontaneous abortus in Leontopithecus rosalia. One fetus (left) had died much earlier. | ||
16) Physiological data No relevant data are reported 17)
Other resources 18)
Additional needs for study References Barnhart, D.D. and Gengozian, N.: An evaluation of the mixed lymphocyte culture reaction in marmosets. Transplantation 20:107-115, 1975. Bedard, M.T., Ma, S.F. and Jones, T.C.: Chromosomal banding patterns and nucleolar organizing regions in three species of Callithricidae (Saguinus oedipus, Saguinus fuscicollis, and Callithrix jacchus). J. Med. primatol. 7:82-97, 1978. Bender, M.A. and Mettler, L.E.: Chromosome studies of primates. II. Callithrix, Leontocebus and Callimico. Cytologia (Tokyo) 25:400-404, 1960. Benirschke, K., Anderson, J.M. and Brownhill, L.E.: Marrow chimerism in marmosets. Science 138:513-515, 1962. Benirschke,
K. and Brownhill, L.E.: Further observations on marrow chimerism in marmosets.
Cytogenetics 2:331-341, 1963. Cadavid, L.F., Shufflebotham, C., Ruiz, F.J., Yeager, M., Hughes, A.L. and Watkins, D.I.: Evolutionary instability of the major histocompatibility complex class I loci in New World primates. Proc. Natl. Acad. Sci. USA 94:14536-14541, 1997. Cell lines inquiries: Dr. Oliver Ryder (oryder@ucsd.edu). Chalifoux, L.V. and Elliott, M.W.:Congenital anomalies in two neonatal tamarins (Saguinus oedipus and Saguinus fuscicollis). J. Med. Primatol. 15:329-337, 1986. Chambers, P.L. and Hearn, J.P.: Embryonic, foetal and placental development in the common marmoset monkey (Callithrix jacchus). J. Zool. London 207:545-561, 1985. Coimbra-Filho, A.F. and Mittermeier, R.A.: New data on the taxonomy of Brazilian marmosets of the genus Callithrix Erxleben, 1777. Folia primatol. 20:241-264, 1973. Coimbra-Filho, A.F. and Mittermeier, R.A., eds.: Ecology and Behavior of Neotropical Primates. Academia Brasileira de Ciências. Rio de Janeiro, 1981. Cooper, R.W.: Small species of primates in biomedical research. Lab. Anim. Care 18:267-279, 1968. Cronin, J.E. and Sarich, V.M.: Molecular systematics of the New World monkeys. J. Human Evol. 4:357-375, 1975. Dunn,
F.L.: Acanthocephalans and cestodes os South American monkeys and marmosets.
J. Parasitol. 49:717-722, 1963. Flurer, C.I. and Zucker, H.: Evaluation of serum parameters relevant to vitamin D status in tamarins. J. Med. Primatol. 16:175-184, 1987. Egozcue,
J., Perkins, E.M. and Hagemenas, F.: Chromosomal evolution in marmosets,
tamarins, and pinchés. Folia Primatol. 9:81-94, 1968. Gengozian, N. and Merritt, C.B.: Effect of unilateral ovariectomy on twinning frequency in the marmoset. J. Reprod. Fert. 23:509-512, 1970. Gengozian, N., Batson, J.S. and Nelson, B.M.: Bone-marrow grafting attempts in marmosets after whole-body irradiation. Int. J. Rad. Biol. 11:553-561, 1966. Gengozian, N., Lushbaugh, C.C., Humason, G.L. and Kniseley, R.M.: "Erythroblastosis foetalis" in the primate, Tamarinus nigricollis. Nature 209:731-732, 1966. Gray, A.P.: Mammalian Hybrids. Commonwealth Agricultural Bureaux, Farnham Royal, Slough SL2 3BN, 1971. Hearn, J.P., Abbott, D.H., Chambers, P.C., Hodges, J.K. and Lunn, S.F.: Use of the common marmoset, Callithrix jacchus, in reproductive research. Prim. Med. 10:40-49, 1978. Hershkovitz, P.: Notes on tertiary platyrrhine monkeys and description of a new genus from the late miocene of Colombia. Folia Primatol. 12:1-37, 1970. Hershkovitz, P.: Comments on the taxonomy of Brazilian marmosets (Callithrix, Callitrichidae). Folia Primatol. 24:137-172, 1975. Hampton, J.K., Hampton, S.H. and Levy, B.M.: Reproductive physiology and pregnancy in marmosets. pp. 527-535 in Medical Primatology, Karger, Basel 1970. Hearn, J.P., Abbott, D.H., Chambers, P.C., Hodges, J.K. and Lunn, S.F.: Use of the common marmoset, Callithrix jacchus, in reproductive research. Prim. Med. 10:40-49, 1978. Karger, Basel. Hobson,
B.M., Hearn, J.P., Lunn, S.F. and Flockhart, J.H.: Urinary excretion of
biologically active chorionic gonadotrophin by the pregnant marmoset (Callithrix
jacchus jacchus). Fol. Primatol. 28:251-258, 1977. Gengozian, N. and Merritt, C.B.: Effect of unilateral ovariectomy on twinning frequency in the marmoset. J. Reprod. Fert. 23:509-512, 1970. Gengozian, N., Batson, J.S. and Nelson, B.M.: Bone-marrow grafting attempts in marmosets after whole-body irradiation. Int. J. Rad. Biol. 11:553-561, 1966. Gengozian, N., Lushbaugh, C.C., Humason, G.L. and Kniseley, R.M.: "Erythroblastosis foetalis" in the primate, Tamarinus nigricollis. Nature 209:731-732, 1966. Gray, A.P.: Mammalian Hybrids. Commonwealth Agricultural Bureaux, Farnham Royal, Slough SL2 3BN, 1971. Hearn, J.P., Abbott, D.H., Chambers, P.C., Hodges, J.K. and Lunn, S.F.: Use of the common marmoset, Callithrix jacchus, in reproductive research. Prim. Med. 10:40-49, 1978. Hershkovitz, P.: Notes on tertiary platyrrhine monkeys and description of a new genus from the late miocene of Colombia. Folia Primatol. 12:1-37, 1970. Hershkovitz, P.: Comments on the taxonomy of Brazilian marmosets (Callithrix, Callitrichidae). Folia Primatol. 24:137-172, 1975. Hampton, J.K., Hampton, S.H. and Levy, B.M.: Reproductive physiology and pregnancy in marmosets. pp. 527-535 in Medical Primatology, Karger, Basel 1970. Hearn, J.P., Abbott, D.H., Chambers, P.C., Hodges, J.K. and Lunn, S.F.: Use of the common marmoset, Callithrix jacchus, in reproductive research. Prim. Med. 10:40-49, 1978. Karger, Basel. Hobson,
B.M., Hearn, J.P., Lunn, S.F. and Flockhart, J.H.: Urinary excretion of
biologically active chorionic gonadotrophin by the pregnant marmoset (Callithrix
jacchus jacchus). Fol. Primatol. 28:251-258, 1977. Hunt,
R.D. and Garcia, F.G.: Hypervitaminosis D in New World monkeys. Am. J.
Clin. Nutrition 22:358-366, 1969. Hunt, R.D., Garcia, F.G. and Hegsted, D.M.: A comparison of vitamin D2 and D3 in New World primates. I. Production and regression of osteodystrophia fibrosa. Lab. Anim. Care 17:222-234, 1967. Jollie, W.P., Haar, J.L. and Craig, S.S.: Fine structural observations on hematopoiesis in the chorioallantoic placenta of the marmoset. Amer. J. Anat. 144:9-38, 1975. Lasley,
B.L., Monfort, S.L., Hodges, J.K. and Czekala, N.M.: Comparison of urinary
estrogens during pregnancy in diverse species. In, Fetal Endocrinology,
pp. 111-126, Academic Press, 1981. Nowak,
R.M. and Paradiso, J.L.: Walker's Mammals of the World, 4th ed. Vol. 1.Johns
Hopkins Univ. Press, Baltimore, 1983. Preslock, J.P., Hampton, S.H. and Hampton, J.K.: Cyclic variations of serum progestins and immunoreactive estrogens in marmosets. Endocrinology 92:1096-1101, 1973. Ryan, K.J., Benirschke, K. and Smith, O.W.: conversion of andro-stenedione-4-C14 to estrone by the marmoset placenta. Endocrinology 69:613-618, 1961 Sarich,
V.M. and Cronin, J.E.: South American mamma molecular systematics, evolutionary
clocks, and continental drift. In, Evolutionary Biology of the New World
Monkeys and Continental Drift. R. Ciochon & A.B. Chiarelli, eds. Plenum
Press, N.Y. 1980. Chapter 20. Seuanez, H.N., L. Forman, L. and Alves, G.: Comparative chromosome morphology in three Callithrichid genera: Cebuella, Callithrix, and Leontopithecus. J. Hered. 79:418-424, 1988. Smith, C.A., Moore, H.D.M. and Hearn, J.P.: The ultrastructure of early implantation in the marmoset monkey (Callithrix jacchus). 175:399-410, 1987. Spatz, W.B.: Nabelschnur-Länge bei Insektivoren und Primaten. Z. Säugetierk. 33:226-239, 1968. Turton, J.A., Ford, D.J., Bleby, J., Hall, B.M. and Whiting, R.: Composition of the milk of the common marmoset (Callithrix jacchus) and milk substitutes used in hand-rearing programmes, with special reference to fatty acids. Fol. Primatol. 29:64-79, 1978. Windle, C.P., Baker, H.F., Ridley, R.M., Oerke, A-K. and Martin, R.D.: Unrearable litters and prenatal reduction of litter size in the common marmoset (Callithrix jacchus). J. Med. Primatol. 28:73-83, 1999. Wislocki,
G.B.: Hematopoiesis in the chorionic villi of the placenta of platyrrhine
monkeys. Anat. Rec. 85:349-363, 1932. Wynn,
R.M., Richards, S.C. and Harris, J.A.: Electron microscopy of the placenta
and related structures of the marmoset. Amer. J. Obstet. Gynecol. 122:60-69,
1975.
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Cottontops (Oedipomidas [Saguinus] oedipus). | ||
Pygmy marmoset (Cebuella pygmaea). Moustached tamarin (Tamarinus nigricollis). | ||
Pygmy marmoset (Cebuella pygmaea). Middle left: Golden lion tamarin (Leontopithecus rosalia). Bottom left: Cotton tops (Oedipomidas [Saguinus] oedipus) Right: Common marmoset (Callithrix jacchus). | ||
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