Accessory Placental Structures—A Review


Many studies have reported on the different types of placenta in different species, but accessory or paraplacental structures are mentioned only in species that have such a nutrient-exchanging mechanism. Hystricomorph rodents possess a subplacenta, swine and equines have the placental areola, equines have the chorionic girdle, and carnivores have hemophagous organs that are equivalent to the placental hematoma in ruminants. These accessory structures are specialized tissues for specific nutrient exchanges in different species, and they are adaptive modifications exhibited by domestic and wild species to remedy the nutritional deficiencies that are related to permeability of the main placenta to important nutrients for the growth and development of the fetus during the gestation.

Share and Cite:

Olio, R. , Lobo, L. , Pereira, M. , Santos, A. , Viana, D. , Favaron, P. and Miglino, M. (2014) Accessory Placental Structures—A Review. Open Journal of Animal Sciences, 4, 305-312. doi: 10.4236/ojas.2014.45039.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Mossman, H.W. (1987) Vertebrate Fetal Membranes: Comparative Ontogeny and Morphology, Evolution, Phylogenetic Significance, Basic Functions, Research Opportunities. Rutgers University Press, New Brunswick.
[2] Amoroso, E.C. (1952) Placentation. In: Parkes, A.S., Ed., Marshall’s Physiology of Reproduction, Longmans Green, London.
[3] Oliveira, M.F., Mess, A., Ambrósio, C.E., Dantas, C.A.G., Favaron, P.O. and Miglino, M.A. (2008) Chorioallantoic Placentation in Galeaspixii (Rodentia, Caviomorpha, Caviidae). Reproductive Biology and Endocrinology, 6, 39.
[4] Davies, J., Dempsey, E.W. and Amoroso, E.C. (1961) The Subplacenta of the Guinea-Pig: Development, Histology and Histochemistry. Journal of Anatomy, 95, 457-473.
[5] Allen, W.R., Hamilton, D.W. and Moor, R.M. (1973) The Origin of Equine Endometrial Cups. II. Invasion of the Endometrium by Trophoblast. The Anatomical Record, 117, 475-501.
[6] Allen, W.R. and Stewart, F. (2001) Equine Placentation. Reproduction, Fertility and Development, 13, 623-634.
[7] Enders, A.C. and Welsh, A.O. (1993) Structural Interactions of Trophoblast and Uterus during Hemochorial Placenta Formation. Journal Experimental Zoology, 266, 578-587.
[8] Leiser, R. and Kaufman, P. (1994) Placental Structure: In a Comparative Aspect. Experimental and Clinical Endocrinology, 102, 122-134.
[9] Mess, A. (2011) Character Transformations and Their Functional Significance as a Key to the Evolution of hystricognathrodentia. Pesquisa Veterinária Brasileira, 31, 1108-1115.
[10] Caixeta, E.S., Fagundes, N.S., Caixeta, M.S. and Pyles, E.S.S. (2008) Desenvolvimento Embrionário Inicial Eqüino-Revisão. Revista Portuguesa de Ciências Veterinárias, 103, 25-34.
[11] Creed, R.F.S. and Biggers, J.D. (1964) Placental Haemophagous Organs in the Procyonidae and Mustelidae. Journal of the Society for Reproduction and Fertility, 8, 133-137.
[12] Pereira, F.T.V., Miglino, M.A., Bevilacqua, E. and Carvalho, A.F. (2001) Aspectos morfológicos dos hematomas placentários da placenta do búfalo (Bubalus bubalis bubalis-Linnaeus, 1758). Brazilian Journal of Veterinary Research and Animal Science, 38, 151-154.
[13] Perrota, C.A. (1959) Fetal Membranes of the Canadian Porcupine, Erithizon dorsatum. The American Journal of Anatomy, 104, 35-59.
[14] Kaufmann, P. and Davidoff, M. (1977) The Guinea Pig Placenta. Advances in Anatomy Embriology and Cell Biology, 53, 5-90.
[15] Roberts, C.M. and Perry, J.S. (1974) Hystricomorph Embriology. Symposia of the Zoological Society of London, 34, 333-360.
[16] Uhlendorf, B. and Kaufmann, P. (1979) Die entwicklung des plazentastieles beim meerschweinchen. Anatomia, Histologia, Embryologia, 8, 233-247.
[17] Hillemann, H.H. and Gaynor, A.I. (1961) The Definitive Architecture of the Placenta of Nutria, Myocastor coypus (Molina). The American Journal of Anatomy, 109, 299-317.
[18] Fischer, T.V. (1985) The Subplacenta of the Beaver (Castor canadensis). Placenta, 6, 311-321.
[19] Soiron, M.L. (1993) Das Siidamerikanische wasserschwein (Hydrochoerus hydrochaeris L. 1766). Ph.D. Dissertation, Fachbereich Veterinãrmedizin, Justus-Liebig-Universitãt Giessen, Giessen.
[20] Kaufmann, P. (2004) Capybara Hydrochaeris Hydrochaeris. Comparative Placentation.
[21] Kanashiro, C., Santos, T.C., Miglino, M.A., Mess, A.M. and Carter, A.M. (2009) Growth and Development of the Placenta in the Capybara (Hydrochaeris hydrochaeris). Reproductive Biology and Endocrinology, 7, 57.
[22] Oliveira, M.F., Carter, A.M., Bonatelli, M., Ambrosio, C.E. and Miglino, M.A. (2005) Placentation in the Rock Cavy, Kerodon rupestris (Wied). Placenta, 27, 87-97.
[23] Miglino, M.A., Carter, A.M., Ferraz, R.H.S. and Machado, M.R.F. (2002) Placentation in the Capybara (Hydrochaerus hydrochaeris), Agouti (Dasyprocta aguti) and Paca (Agouti paca). Placenta, 23, 416-428.
[24] Oliveira, M.F., Favaron, P.O., Ambrósio, C.E., Miglino, M.A. amd Mess, A.M. (2012) Chorioallantoic and Yolk Sac Placentation in Thrichomys laurentinus (Echimyidae) and the Evolution of Hystricognath Rodents. Journal of Experimental Zoology. Part B: Molecular and Developmental Evolution, 318, 13-25.
[25] Fischer, T.V. and Floyd, A.D. (1972) Placental Development in the Mongolian Gerbil (Meriones unguiculatus). II. From the Establishment of the Labyrinth to Term. American Journal of Anatomy, 134, 321-335.
[26] Duval, M. (1892) Le Placenta des Rongeurs. Le placenta ducochon d’Inde. Journal of Anatomy (Paris), 28, 58-408.
[27] Minot, C. (1889) Uterus and Embryo: I. Rabbit; II. Man. Harvard Medical School, Boston, Mass. Reprinted The Journal of Morphology, 2.
[28] Mossman, H.W. (1991) Classics Revisited: The Comparative Morphogenesis of the Foetal Membranes and Accessory Uterine Structures. Placenta, 12, 1-5.
[29] Rodrigues, R.F., Carter, A.M., Ambrósio, C.E., Santos, T.C. and Miglino, M.A. (2006) The Subplacenta of the Red-Rumped Agouti (Dasyprocta leporina L). Reproductive Biology and Endocrinology, 4, 31.
[30] Mess, A. (2003) Evolutionary Transformations of Chorioallantoic Placental Characters in Rodentia with Special Reference to Hystricognath Species. Journal of Experimental Zoology, 299A, 78-98.
[31] Carter, A.M. (2001) Evolution of the Placenta and Fetal Membranes Seen in the Light of Molecular Phylogenetics. Placenta, 22, 800-807.
[32] Carter, A.M. (2007) Animal Models of Human Placentation—A Review. Placenta, 28, S41-S47.
[33] Friess, A.E., Sinowatz, F., Skolek-Winnisch, R. and Traütner, W. (1981) The Placenta of the Pig. II. The Ultrastructure of the Areola. Anatomy and Embryology, 163, 43-53.
[34] Dantzer, V. and Leiser, R. (1993) Microvasculature of Regular and Irregular Areolae of the Areola-Gland Subunit of the Porcine Placenta: Structural and Functional Aspects. Anatomy and Embryology, 188, 257-267.
[35] Miglino, M.A., Pereira, F.T.V., Santos, T.C. and Carvalho, A.F. (2001) A morfologia placentária dos suínos domés-ticos. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR, 4, 71-76.
[36] Abd-Elnaeim, M., Leiser, R. and Allen, W.R. (2003) Structural and Haematological Aspects of the Equine Placenta in Mid-Pregnancy. Havemeyer Foundation Monograph Series, 10, 39-42.
[37] Wooding, F.B.P., Morgan, G., Fowden, A.L. and Allen, W.R. (2000) Separate Sites and Mechanisms for Placental Transport of Calcium, Iron and Glucose in the Equine Placenta. Placenta, 21, 635-645.
[38] Bazer, F.W., Vallet, J.L., Roberts, R.M., Sharp, D.C. and Thatcher, W.W. (1986) Role of Conceptus Secretory Products in Establishment of Pregnancy. Journal of the Society for Reproduction and Fertility, 76, 841-850.
[39] Bazer, F.W. (1975) Uterine Protein Secretions: Relationship to Development of the Conceptus. Journal of Animal Science, 41, 1376-1382.
[40] Chen, T.T., Bazer, F.W., Gebhardt, B.M. and Roberts, R.M. (1975) Uterine Secretion in Mammals: Synthesis and Placental Transport of a Purple Acid Phosphatase in Pigs. Biology of Reproduction, 13, 304-313.
[41] Raub, T.J., Bazer, F.W. and Roberts, R.M. (1985) Localization of the Iron Transport Glycoprotein, Uteroferrin, in the Porcine Endometrium and Placenta by Using Immunocolloidal Gold. Anatomy and Embryology, 171, 253-258.
[42] Mançanares, A.C.F., Mançanares, C.A.F., Franciolli, A.L.R., Marques, L.O., Ambrósio, C.E., Miglino, M.A. and Carvalho, A.F. (2012) Relação entre a quantidade de AgNORS, atividade proliferativa e o estágio de desenvolvimento placentário em equinos. Pesquisa Veterinária Brasileira, 32, 08-112.
[43] Lunn, P., Vagnani, K.E. and Ginther, O.J. (1996) The Equine Immune Response to Endometrial Cups. Journal of Reproductive Immunology, 34, 203-216.
[44] Silva, E.S.M., Filho, J.N.P.P. and Meira, C. (2012) Aspectos relacionados à formação, função e regressão dos corpos lúteos suplementares em éguas. Veterinária e Zootecnia, 19, 283-293.
[45] Stewart, F. and Allen, W.R. (1981) Biological Functions and Receptor Binding Activities of Equine Chorionic Gonadotrophins. Journal of the Society for Reproductive and Fertility, 62, 527-536.
[46] Barnes, F.W. (2000) The Effects of the Early Uterine Environment on the Subsequent Development of Embryo and Fetus. Theriogenology, 53, 649-658.
[47] Costa, L.L., Silva, J.C. and Silva, J.R. (2001) Superovulatory Response, Embryo Quality and Fertility after Treatment with Different Gonadotrophins in Native Cattle. Theriogenology, 56, 65-77.
[48] Baruselli, P.S., Jacomini, J.O., Sales, J.N.S. and Crepaldi, G.A. (2008) Importancia do emprego da eCG em protocolos de sincronização para IA, TE e SOV em tempo fixo. Biotechnology of Reproduction in Bovines 3rd International Symposium of Applied Animal Reproduction, 146-167.
[49] Biggers, J.D. and Creed, R.F.S. (1962) Two Morphological Types of Placentae in the Raccoon. Nature, 194, 103-105.
[50] Creed, R.F.S. and Biggers, J.D. (1963) Some Aspects of Placental Structure in the Raccoon (Procyon lotor L.). Journal of Anatomy, 97, 475.
[51] Creed, R.F.S. and Biggers, J.D. (1963) Development of the Raccoon Placenta. American Journal of Anatomy, 113, 417-445.
[52] Perry, J.P. (1981) The Mammalian Fetal Membranes. Journal of the Society for Reproduction and Fertility, 62, 321-335.
[53] Myagkaya, G.L., Schonargel, K., Van veen, H. and Everts, V. (1984) Electron Microscopic Study of the Localization of Ferric Iron in Chorionic Epithelium of the Sheep Placenta. Placenta, 5, 551-558.
[54] King, B.F. (1993) Comparative Anatomy of Placental Barrier. Bibliotheca Anatomica (Karger, Brasil), 22, 13-28.
[55] McArdle, H.J., Danzeisen, R., Forret, C. and Gambling, L. (2003) The Role of the Placenta in Iron Transfer from Mother to Fetus and the Relationship between Iron Status and Fetal Outcone. Biometals, 16, 161-167.
[56] Godfrey, K.M. and Barker, D.J.P. (2000) Fetal Nutrition and Adult Disease. Journal Experimental Zoology, 299A, 78-98.
[57] Pereira, F.T.V., Braga, F.C., Burioli, K.C., Kfoury Junior, J.R., Oliveira, L.J., Papa, P.C., Carvalho, A.F., Ambrósio, C.E., Bazer, F.W. and Miglino, M.A. (2010) Transplacental Transfer of Iron in the Water Buffalo (Bubalus bubalis): Uteroferrin and Erythrophagocytosis. Reproduction in Domestic Animals, 45, 907-914.

Copyright © 2021 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.