Term ovine placental vasculature: Comparison of sea level and high altitude conditions by corrosion cast and histomorphometry
Abstract
The placental vascular architecture differs significantly at high altitude from that at sea level in the human and guinea-pig. Four sheep between 137 and 140 days of gestation, kept near sea level throughout gestation, were used as a normoxic control group for comparison of the placental vasculature with 10 other ewes, kept at high altitude (3820 m above sea level; Barcroft Laboratory, White Mountain Research Station, CA, USA). Placentomes from both groups were prepared for histology and scanning electron microscopy of vascular corrosion casts. Singular perfusion of fetal placentae, as well as combined maternal/fetal injection was performed. The influence of long-term hypoxaemia was determined by qualitative and semi-quantitative evaluation of corrosion casts and histological sections. The fetal vessel casts show a distinct difference in the arrangement of vessels of all sizes in response to long-term hypoxaemia. In the control group, stem arteries and veins are straight and parallel. In contrast, this is much less evident in the hypoxaemic group because arterioles and venules branch off the stem vessels more frequently and in an irregular manner. This leads to a capillary bed that is much more dense due to increased branching and capillary coiling. These observations are confirmed by histomorphometry. In the fetal vessels of high altitude sheep placentomes, we observed a decreased number of vascular cross sections (21.6 +/- 4.7 SEM versus 27.7 +/- 4.0 SEM; P = 0.02). However, the average luminal size per cross section (77.9 +/- 10.5 microns2 SEM versus 59.4 +/- 7.4 microns2 SEM; P = 0.004) was increased at high altitude and the percentage of lumina of the total area (5.7 +/- 0.5 SEM versus 5.3 +/- 0.3 SEM; P = 0.09) indicated a trend towards an increase. In maternal vessels of high altitude placentomes, the number of vessel cross sections (6.5 +/- 0.7 SEM versus 6.0 +/- 0.5 SEM; P = 0.2) remained unchanged, whereas the average luminal size (1108 +/- 122 microns2 SEM versus 844 +/- 77 microns2 SEM; P < 0.001) and the percentage of lumina out of the total area (20.9 +/- 1.8 SEM versus 17.5 +/- 1.7 SEM; P < 0.001) were increased. The interhaemal distance appeared to be slightly but not significantly increased at high altitude. These findings indicate that at high altitude the sheep placenta develops an increased materno-fetal absorptive surface to help guarantee substance exchange.
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At high altitude, there are changes in the vasculature and blood flow on the fetal side of the placenta in both humans and sheep.
“At high altitude, there are also changes in the vasculature and blood flow on the fetal side of the placenta in both humans and sheep (317, 431, 443).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [317]
In pregnant sheep at high altitude, the luminal cross sectional area, but not the number, of maternal vessels in the placentomes is increased, which results in a greater percentage area of maternal blood vessels and normal fetal growth.
“In pregnant sheep at high altitude, the luminal cross sectional area, but not the number, of maternal vessels in the placentomes is increased, which results in a greater percentage area of maternal blood vessels and normal fetal growth (317, 437).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [317]
In neither mouse nor sheep is there evidence for thinning of the interhemal membrane in response to hypoxic conditions.
“In neither of these species is there evidence for thinning of the interhemal membrane in response to hypoxic conditions (133, 317).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [317]
Similar increases in fetal vascularity are seen in ovine placentomes at high altitude, but, in contrast to the findings in the human placenta, these are accompanied by an increase in the total surface area of fetal-maternal contact for gas exchange.
“Similar increases in fetal vascularity are seen in ovine placentomes at high altitude, but, in contrast to the findings in the human placenta, these are accompanied by an increase in the total surface area of fetal-maternal contact for gas exchange (317, 431).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [317]
Cites
The Pathology of the Human Placenta
Benirschke, K., & Driscoll, S. G. (1967) · Springer eBooks · doi:10.1007/978-1-4612-9809-0 · Cited by 2,123 · see citing works
Marshall’s Physiology of Reproduction
Lamming, G. E. (1994) · Springer eBooks · doi:10.1007/978-94-011-1286-4 · Cited by 1,377 · see citing works
(1973) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-3288-6 · Cited by 708 · see citing works
Pathology of the Human Placenta
Benirschke, K., & Kaufmann, P. (1990) · Springer eBooks · doi:10.1007/978-1-4757-4193-3 · Cited by 689 · see citing works
The synepitheliochorial placenta of ruminants: Binucleate cell fusions and hormone production
Wooding, F. B. P. (1992) · Placenta · doi:10.1016/0143-4004(92)90025-o · Cited by 503 · see citing works
Placental structure: in a comparative aspect
Leiser, R., & Kaufmann, P. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1211275 · Cited by 452 · see citing works
Self-citationJunqueira, L. C. D. S., Carneiro, J., Schiebler, T. H., & Peiper, U. (1984) · Springer eBooks · doi:10.1007/978-3-662-21996-6_2 · Cited by 349 · see citing works
Angiogenesis in the female reproductive system
Reynolds, L. P., Killilea, S. D., & Redmer, D. A. (1992) · The FASEB Journal · doi:10.1096/fasebj.6.3.1371260 · Cited by 346 · see citing works
Angiogenesis in female reproductive system
Longjiang, Shao, S., Cheng, & Zhu (2001) · 中国科学通报:英文版 · Cited by 339 · see citing works
(1988) · Placenta · doi:10.1016/0143-4004(88)90060-4 · Cited by 319 · see citing works
A HISTOLOGICAL AND HISTOCHEMICAL EXAMINATION OF IMPLANTATION AND EARLY PLACENTOME FORMATION IN SHEEP
Boshier, D. P. (1969) · Reproduction · doi:10.1530/jrf.0.0190051 · Cited by 249 · see citing works
Frühentwicklung, Eihautbildung und Placentation des Menschen und der Säugetiere
Großer, O. (1927) · Medical Entomology and Zoology · Cited by 228 · see citing works
The fetal vascularisation of term human placental villi
Kaufmann, P., Bruns, U., Leiser, R., Luckhardt, M., & Winterhager, E. (1985) · Anatomy and Embryology · doi:10.1007/bf00316301 · Cited by 170 · see citing works
Self-citationBurton, G. J., Reshetnikova, O. S., Milovanov, A. P., & Teleshova, O. V. (1996) · Placenta · doi:10.1016/s0143-4004(05)80643-5 · Cited by 149 · see citing works
Handbook of Physiology: Section 3: Respiration. Volume 1
Fenn, W. O., & Rahn, H. (1965) · Anesthesiology · doi:10.1097/00000542-196505000-00022 · Cited by 134 · see citing works
Reshetnikova, O. S., Burton, G. J., & Milovanov, A. P. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(94)90402-2 · Cited by 127 · see citing works
Jackson, M. R., Mayhew, T. M., & Haas, J. D. (1987) · Placenta · doi:10.1016/0143-4004(87)90077-4 · Cited by 112 · see citing works
Comparative placentation : essays in structure and function
Steven, D. H. (1975) · Academic Press eBooks · Cited by 106 · see citing works
Placental anatomy and diffusing capacity in guinea pigs following long-term maternal hypoxia
Bacon, B. J., Gilbert, R. D., Kaufmann, P., Smith, A. D., Trevino, F. T., & Longo, L. D. (1984) · Placenta · doi:10.1016/s0143-4004(84)80002-8 · Cited by 96 · see citing works
Current topic: Comparative physiology of placental oxygen transport
Wilkening, R. B., & Meschia, G. (1992) · Placenta · doi:10.1016/0143-4004(92)90002-b · Cited by 82 · see citing works
Barcroft, J., & Barron, D. H. (1946) · The Anatomical Record · doi:10.1002/ar.1090940403 · Cited by 82 · see citing works
Reshetnikova, O. S., Burton, G. J., Milovanov, A. P., & Fokin, E. I. (1996) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(96)70427-1 · Cited by 77 · see citing works
Oxygen diffusive conductances of human placentae from term pregnancies at low and high altitudes
Mayhew, T. M., Jackson, M. R., & Haas, J. D. (1990) · Placenta · doi:10.1016/s0143-4004(05)80195-x · Cited by 77 · see citing works
Some aspects of the comparative anatomy of the mammalian placenta
Wimsatt, W. A. (1962) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(62)90004-2 · Cited by 76 · see citing works
Placental physiology: Structure and function of fetomaternal exchange
Faber, J. J., & Thornburg, K. L. R. (1983) · Medical Entomology and Zoology · Cited by 75 · see citing works
Mechanism of glucose transport across the human and rat placental barrier: A review
Takata, K., & Hirano, H. (1997) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19970701/15)38:1/2 · Cited by 72 · see citing works
Self-citationJackson, M., Mayhew, T. M., & Haas, J. D. (1987) · PubMed · Cited by 72 · see citing works
The fetal vascularisation of term human placental villi
Leiser, R., Luckhardt, M., Kaufmann, P., Winterhager, E., & Bruns, U. (1985) · Anatomy and Embryology · doi:10.1007/bf00707305 · Cited by 69 · see citing works
Self-citationRespiratory Function of the Placenta as Determined with Carbon Monoxide in Sheep and Dogs*
Longo, L. D., Power, G. G., & Forster, R. E. (1967) · Journal of Clinical Investigation · doi:10.1172/jci105581 · Cited by 68 · see citing works
The development of the placenta in the sheep and goat: an electron microscope study.
Lawn, A. M., Chiquoine, A. D., & Amoroso, E. C. (1969) · PubMed · Cited by 66 · see citing works
Jackson, M. R., Joy, C. F., Mayhew, T. M., & Haas, J. D. (1985) · Placenta · doi:10.1016/s0143-4004(85)80054-0 · Cited by 65 · see citing works
Theoretical analysis of factors affecting placental O 2 transfer
Longo, L., Hill, E., & Power, G. (1972) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1972.222.3.730 · Cited by 65 · see citing works
Challis, J. R. G., Fraher, L., Oosterhuis, J., White, S. E., & Socking, A. D. (1989) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(89)90312-8 · Cited by 61 · see citing works
Placental Physiology: Structure and Function of Fetomaternal Exchange
Evans, A. T. (1984) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(12)61474-8 · Cited by 60 · see citing works
Oxygen Transport to Tissue XII
Piiper, J., Goldstick, T. K., & Meyer, M. (1990) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-8181-5 · Cited by 59 · see citing works
Chorangiosis and chorangioma in three cohorts of placentas from Nepal, Tibet, and Japan
Soma, H., Watanabe, Y., & Hata, T. (1995) · Reproduction, Fertility and Development · doi:10.1071/rd9951533 · Cited by 58 · see citing works
Jackson, M. R., Mayhew, T. M., & Haas, J. D. (1988) · Placenta · doi:10.1016/0143-4004(88)90068-9 · Cited by 57 · see citing works
Observation on the fine structure of the sheep placenta
Davies, J., & Wimsatt, W. A. (2008) · Acta Anatomica · doi:10.1159/000142872 · Cited by 54 · see citing works
Developments in ultrastructure of reproduction
(1990) · General and Comparative Endocrinology · doi:10.1016/0016-6480(90)90218-b · Cited by 54 · see citing works
Blood Flow and Steroid and Nutrient Uptake of the Gravid Uterus and Fetus of Sows1
Reynolds, L. P., Ford, S. P., & Ferrell, C. L. (1985) · Journal of Animal Science · doi:10.2527/jas1985.614968x · Cited by 51 · see citing works
Comparative Morphological Aspects of Placental Vascularization
Dantzer, V., Leiser, R., Kaufmann, P., & Luckhardt, M. (1988) · Springer eBooks · doi:10.1007/978-1-4615-8109-3_17 · Cited by 49 · see citing works
Self-citationLeiser, R., & Kohler, T. (1984) · Anatomy and Embryology · doi:10.1007/bf00319006 · Cited by 46 · see citing works
Self-citationFINE STRUCTURE OF THE OVINE PLACENTOME.
Bjoerkman, N. (1965) · PubMed · Cited by 45 · see citing works
Placental diffusing capacity for carbon monoxide and oxygen in unanesthetized sheep
Longo, L. D., & Ching, K. S. (1977) · Journal of Applied Physiology · doi:10.1152/jappl.1977.43.5.885 · Cited by 43 · see citing works
Leiser, R., & Kohler, T. (1983) · Anatomy and Embryology · doi:10.1007/bf00304602 · Cited by 43 · see citing works
Self-citationAlterations of the Fetal Capillary Bed in the Guinea Pig Placenta Following Long-Term Hypoxia
Scheffen, I., Kaufmann, P., Philippens, L., Leiser, R., Geisen, C., & Mottaghy, K. (1990) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-8181-5_89 · Cited by 41 · see citing works
Self-citationThe Development of the Brain and its Disturbance by Harmful Factors
Macrae, D. (1964) · Postgraduate Medical Journal · doi:10.1136/pgmj.40.464.358-c · Cited by 36 · see citing works
Olivo, M., Bhardwaj, R. S., Schulze‐Osthoff, K., Sorg, C., Jacob, H. J., & Flamme, I. (1992) · The Anatomical Record · doi:10.1002/ar.1092340112 · Cited by 36 · see citing works
Fetal breathing adaptation to prolonged hypoxaemia in sheep.
Koos, B. J., Kitanaka, T., Matsuda, K., Gilbert, R. D., & LONGO, L. D. (1988) · PubMed · Cited by 31 · see citing works
Zur Feinstruktur der materno-fetalen Verbindung im Placentom des Schafes (Ovis aries L.)
Ludwig, K. S. (1962) · Cellular and Molecular Life Sciences · doi:10.1007/bf02148304 · Cited by 28 · see citing works
Fetal Vasculature of the Human Placenta: Scanning Electron Microscopy of Microvascular Casts
Leiser, R. (1985) · Contributions to gynecology and obstetrics · doi:10.1159/000410666 · Cited by 21 · see citing works
Self-citationMaternal and fetal vascular nets in placentas of sheep and goats
Makowski, E. L. (1968) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)33734-0 · Cited by 20 · see citing works
Placentaver�nderungen bei EPH-Gestose
H�lzl, M., L�thje, D., & Seck-Ebersbach, K. (1974) · Archives of Gynecology and Obstetrics · doi:10.1007/bf00669739 · Cited by 18 · see citing works
Leiser, R., Dantzer, V., & Kaufmann, P. (1989) · PubMed · Cited by 13 · see citing works
Self-citationKaufmann, P., Kohnen, G., & Kosanke, G. (1993) · PubMed · Cited by 10 · see citing works
Comparative physiology of placental oxygen transport
Wilkening, R. B., & Meschia, G. (1992) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(92)90316-b · Cited by 7 · see citing works
Willard, P. W. (1962) · Archives of Surgery · doi:10.1001/archsurg.1962.01300230041009 · Cited by 5 · see citing works
Effect of Long-Term Hypoxia on Oxygen Transport Properties of Blood in Pregnant Guinea Pigs
Geisen, C., Mottaghy, K., Scheffen, I., & Kaufmann, P. (1990) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-8181-5_88 · Cited by 5 · see citing works
Flagged first, then by citations
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Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
Jansson, T., & Powell, T. L. (2007) · Clinical Science · doi:10.1042/cs20060339 · Cited by 542 · see citing works
Evidence for altered placental blood flow and vascularity in compromised pregnancies
Reynolds, L. P., Caton, J. S., Redmer, D. A., Grazul‐Bilska, A. T., Vonnahme, K. A., Borowicz, P. P., Luther, J. S., Wallace, J. M., Wu, G., & Spencer, T. E. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.104430 · Cited by 358 · see citing works
Ahmed, A. M., Dunk, C., Ahmad, S., & Khaliq, A. (2000) · Placenta · doi:10.1053/plac.1999.0524 · Cited by 349 · see citing works
Mayhew, T. M., Jones, D. S., & Kaufmann, P. (2003) · Placenta · doi:10.1016/j.placenta.2003.10.010 · Cited by 328 · see citing works
The Role of the Placenta in Fetal Programming—A Review
Godfrey, K. M. (2002) · Placenta · doi:10.1053/plac.2002.0773 · Cited by 305 · see citing works
Placental Development in Normal and Compromised Pregnancies— A Review
Regnault, T. R. H., Galan, H. L., Parker, T. A., & Anthony, R. V. (2002) · Placenta · doi:10.1053/plac.2002.0792 · Cited by 264 · see citing works
Hoet, J. J., & Hanson, M. A. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.617ad.x · Cited by 232 · see citing works
Bertolini, M., Mason, J. B., Beam, S. W., Carneiro, G. F., Sween, M. L., Kominek, D. J., Moyer, A. L., Famula, T. R., Sainz, R. D., & Anderson, G. B. (2002) · Theriogenology · doi:10.1016/s0093-691x(02)00935-4 · Cited by 204 · see citing works
Placental angiogenesis in sheep models of compromised pregnancy
Reynolds, L. P., Borowicz, P. P., Vonnahme, K. A., Johnson, M. L., Grazul‐Bilska, A. T., Redmer, D. A., & Caton, J. S. S. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.081745 · Cited by 154 · see citing works
Gene expression in the placenta: maternal stress and epigenetic responses
Gheorghe, C. P., Goyal, R., Mittal, A., & Longo, L. D. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082770cg · Cited by 150 · see citing works
The carnivore pregnancy: The development of the embryo and fetal membranes
Miglino, M. A., Ambrósio, C. E., Martins, D. D. S., Wenceslau, C. V., Pfarrer, C. D., & Leiser, R. (2006) · Theriogenology · doi:10.1016/j.theriogenology.2006.02.027 · Cited by 124 · see citing works
Self-citationRumball, C. W. H., Harding, J. E., Oliver, M. H., & Bloomfield, F. H. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.144071 · Cited by 87 · see citing works
Ovine placentome morphology: Effect of high altitude, long-term hypoxia
Penninga, L., & Longo, L. D. (1998) · Placenta · doi:10.1016/s0143-4004(98)90008-x · Cited by 82 · see citing works
Placental Gas Exchange and the Oxygen Supply to the Fetus
Carter, A. M. (2015) · Comprehensive physiology · doi:10.1002/cphy.c140073 · Cited by 77 · see citing works
Mayhew, T. M. (2003) · Placenta · doi:10.1053/plac.2002.0895 · Cited by 75 · see citing works
Fetal villosity and microvasculature of the bovine placentome in the second half of gestation
Leiser, R., Krebs, C., Klisch, K., Ebert, B., Dantzer, V., Schuler, G. C., & Hoffmann, B. (1997) · Journal of Anatomy · doi:10.1046/j.1469-7580.1997.19140517.x · Cited by 75 · see citing works
Self-citationZhang, E., Burton, G. J., Smith, S. K., & Jones, D. S. (2002) · Placenta · doi:10.1053/plac.2002.0856 · Cited by 67 · see citing works
Darby, J. R. T., Varcoe, T. J., Orgeig, S., & Morrison, J. L. (2020) · Theriogenology · doi:10.1016/j.theriogenology.2020.01.080 · Cited by 60 · see citing works
Gene Expression Patterns in the Hypoxic Murine Placenta: A Role in Epigenesis?
Gheorghe, C. P., Mohan, S., Oberg, K. C., & Longo, L. D. (2007) · Reproductive Sciences · doi:10.1177/1933719107302860 · Cited by 51 · see citing works
Maternal Stress and Placental Vascular Function and Remodeling
Reynolds, L. P., Vonnahme, K. A., Lemley, C. O., Redmer, D. A., Grazul‐Bilska, A. T., Borowicz, P. P., & Caton, J. S. S. (2013) · Current Vascular Pharmacology · doi:10.2174/1570161111311050003 · Cited by 50 · see citing works
Architecture of Normal Villous Trees
Benirschke, K., Burton, G. J., & Baergen, R. N. (2012) · Springer eBooks · doi:10.1007/978-3-642-23941-0_7 · Cited by 50 · see citing works
Steyn, C., Hawkins, P., Saito, T., Noakes, D. E., Kingdom, J. C., & Hanson, M. A. (2001) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(01)00321-9 · Cited by 47 · see citing works
Pfarrer, C. D., Ebert, B., Miglino, M. A., Klisch, K., & Leiser, R. (2001) · Journal of Anatomy · doi:10.1046/j.1469-7580.2001.19850591.x · Cited by 47 · see citing works
Self-citationInvestigating developmental cardiovascular biomechanics and the origins of congenital heart defects
Kowalski, W. J., Pekkan, K., Tinney, J. P., & Keller, B. B. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00408 · Cited by 43 · see citing works
Maternal environment and placental vascularization in small ruminants
Bairagi, S., Quinn, K. E., Crane, A. R., Ashley, R. L., Borowicz, P. P., Caton, J. S., Redden, R. R., Grazul‐Bilska, A. T., & Reynolds, L. P. (2016) · Theriogenology · doi:10.1016/j.theriogenology.2016.04.042 · Cited by 42 · see citing works
Do we now understand the control of the fetal circulation?
Hanson, M. A. (1997) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(97)00203-0 · Cited by 37 · see citing works
Kingdom, J. C. (1998) · Placenta · doi:10.1016/s0143-4004(98)90073-x · Cited by 36 · see citing works
Parraguez, V. H., Atlagich, M., Díaz, R., Cepeda, R., González, C., Reyes, M. D. L., Bruzzone, M. E., Behn, C., & Raggi, L. A. (2005) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2005.11.003 · Cited by 35 · see citing works
Placentation in the alpaca Lama pacos
Olivera, L., Zago, D., Leiser, R., Jones, C. J. P., & Bevilacqua, E. M. A. F. (2003) · Anatomy and Embryology · doi:10.1007/s00429-003-0328-3 · Cited by 35 · see citing works
Self-citationWood, C. E., & KELLER-WOOD, M. E. (2019) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00008.2019 · Cited by 34 · see citing works
Hu, X., Chen, M., Dasgupta, C., Xiao, D., Huang, X., Yang, S., & Zhang, L. (2017) · Biology of Reproduction · doi:10.1095/biolreprod.116.145946 · Cited by 33 · see citing works
Jirkovská, M., Kubínová, L., Krekule, I., & HACH, P. (1998) · Anatomy and Embryology · doi:10.1007/s004290050136 · Cited by 32 · see citing works
Ansari, T. (2003) · Placenta · doi:10.1016/s0143-4004(03)00044-4 · Cited by 29 · see citing works
Early influences on embryonic and placental growth
Robinson, J. S., Hartwich, K. M., Walker, S., Erwich, J., & Owens, J. A. (1997) · Acta Paediatrica · doi:10.1111/j.1651-2227.1997.tb18401.x · Cited by 29 · see citing works
Kakabadze, A., & Kakabadze, Z. (2015) · Transplantation Proceedings · doi:10.1016/j.transproceed.2014.09.181 · Cited by 27 · see citing works
West, R. C., Bouma, G. J., & Winger, Q. A. (2018) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-018-0421-3 · Cited by 26 · see citing works
The Placenta in Toxicology. Part I
Buse, E., Häeger, J.-D., Svensson‐Arvelund, J., Markert, U. R., Faas, M. M., Ernerudh, J., Dixon, D., Cline, J. M., & Pfarrer, C. D. (2013) · Toxicologic Pathology · doi:10.1177/0192623313482208 · Cited by 17 · see citing works
Abd-Elnaeim, M. M. M., Miglino, M. A., Pfarrer, C. D., & Leiser, R. (2003) · Annals of Anatomy - Anatomischer Anzeiger · doi:10.1016/s0940-9602(03)80053-5 · Cited by 16 · see citing works
Self-citationArroyo, J. A., Anthony, R. V., & Galan, H. L. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.12.017 · Cited by 16 · see citing works
Cell cycle and apoptosis in normal and cloned bovine near-term placentae
Rici, R. E. G., Facciotti, P. R., Ambrósio, C. E., Maria, D. A., Kfoury, J. R., Bertolini, M., & Miglino, M. A. (2008) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2008.11.015 · Cited by 16 · see citing works
Placental Defects in α7 Integrin Null Mice
Welser, J. V., Lange, N., Flintoff‐Dye, N. L., Burkin, H. R., & Burkin, D. J. (2007) · Placenta · doi:10.1016/j.placenta.2007.08.002 · Cited by 15 · see citing works
Microscopic anatomy of the ungulate placenta
Macdonald, A. A., & Fowden, A. L. (1997) · Equine Veterinary Journal · doi:10.1111/j.2042-3306.1997.tb05072.x · Cited by 13 · see citing works
The placental gateway of maternal transgenerational epigenetic inheritance
Sailasree, P., Srivastava, S., & Mishra, R. K. (2017) · Journal of Genetics · doi:10.1007/s12041-017-0788-5 · Cited by 12 · see citing works
Growth Factor Regulators of Placental Angiogenesis
Dunk, C., & Ahmed, A. (2000) · Springer eBooks · doi:10.1007/978-1-4471-0735-4_8 · Cited by 11 · see citing works
Yates, D. T., Chen, X., & Limesand, S. W. (2012) · Wiley eBooks · doi:10.1002/9781119949091.ch12 · Cited by 11 · see citing works
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Watson, C. M., & Cox, C. L. (2021) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.23072 · Cited by 10 · see citing works
Classification of Villous Maldevelopment
Benirschke, K., & Kaufmann, P. (2000) · Springer eBooks · doi:10.1007/978-1-4757-4199-5_15 · Cited by 9 · see citing works
Vascularization of the Placenta
Torry, R. J., Schwartz, J. R., & Torry, D. S. (2002) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4612-0109-0_11 · Cited by 8 · see citing works
Analysis of Fetal and Maternal Microvasculature in Ruminant Placentomes by Corrosion Casting
Leiser, R., & Pfarrer, C. D. (2005) · Humana Press eBooks · doi:10.1385/1-59259-983-4:391 · Cited by 7 · see citing works
Self-citationAspectos anatômicos da macro e microvascularização da placenta em ovinos (Ovis aries)
Schoenau, L. S. F., de Morais‐Pinto, L., Pereira, F. T. V., Schoenau, W., & Miglino, M. A. (2005) · Brazilian Journal of Veterinary Research and Animal Science · doi:10.11606/issn.1678-4456.bjvras.2005.26398 · Cited by 6 · see citing works
Britt, J. L., Powell, R. R., McMahan, C. L., Bruce, T. F., & Duckett, S. K. (2021) · Journal of Histotechnology · doi:10.1080/01478885.2021.1902670 · Cited by 5 · see citing works
Respiration in the Fetal-Placental Unit
Rothstein, R. W., & Longo, L. D. (1998) · Springer eBooks · doi:10.1007/978-1-4612-1642-1_23 · Cited by 5 · see citing works
Architecture of Normal Villous Trees
Benirschke, K., & Kaufmann, P. (2000) · Springer eBooks · doi:10.1007/978-1-4757-4199-5_7 · Cited by 5 · see citing works
Jones, D. S., Jauniaux, E. R. M., & Burton, G. J. (2021) · Springer eBooks · doi:10.1007/978-3-030-84725-8_9 · Cited by 4 · see citing works
Control of fetal metabolism: relevance to developmental origins of health and disease
Fowden, A. L., Ward, J. W., & Forhead, A. J. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511544699.011 · Cited by 4 · see citing works
Maternal Stress-Mediated Gene Expression Changes in the Mouse Placenta
Longo, L. D., & Goyal, R. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-394445-0.00037-0 · Cited by 3 · see citing works
FTY720, a sphingosine analog, altered placentome histoarchitecture in ewes
Dunlap, K. A., White, B. G., Erikson, D. W., Satterfield, M. C., Pfarrer, C. D., Wu, G., Bazer, F. W., Burghardt, R. C., Bayless, K. J., & Johnson, G. A. (2020) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-019-0411-0 · Cited by 3 · see citing works
The perinatal llama immersed in the thin oxygen of the Andean Altiplano
Llanos, A. J., Herrera, E. A., Reyes, V. R., Ebensperger, G., & Giussani, D. A. (2025) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2024.0180 · Cited by 2 · see citing works
Architecture of Normal Villous Trees
(2006) · Springer eBooks · doi:10.1007/0-387-26742-5_7 · Cited by 2 · see citing works
Placental Functional Morphology
Burton, G. J. (2001) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4612-0213-4_15 · Cited by 2 · see citing works
Miluska Navarrete, Z., Acuña, F., da Silva, M. D., da Silva, T. S., Garcia, M. H. H., Barreto, R. D. S. N., Sato, A. S., Barbeito, C. G., & Miglino, M. A. (2025) · Biology · doi:10.3390/biology14010064 · Cited by 1 · see citing works
Fetal Growth Restriction at High Altitude: Basic Cellular and Subcellular Physiologic Considerations
Longo, L. D. (2018) · Springer eBooks · doi:10.1007/978-1-4939-7483-2_15 · Cited by 1 · see citing works
Amino acids in sheep production
McCoard, S. A. (2015) · Frontiers in Bioscience-Elite · doi:10.2741/766 · Cited by 1 · see citing works
Placental Vascularity: A Story of Survival
Ford, S. P. (2009) · Springer eBooks · doi:10.1007/978-90-481-3135-8_8 · Cited by 1 · see citing works
Maternal brachycephaly only does not influence umbilical artery resistance in late canine pregnancy
Sandes, V. N. F. G., Mendonça, L. B. R., & Câmara, D. R. (2021) · Medicina Veterinária (UFRPE) · doi:10.26605/medvet-v15n2-4400
Classification of Villous Maldevelopment
(2006) · Springer eBooks · doi:10.1007/0-387-26742-5_15
Aspectos básicos de la reproducción de la vaca
Góngora-Orjuela, A., & Vasquéz, A. H. (2015) · doi:10.22579/9789588927718
- Authors
- Krebsa, C., Longob, L. D., & Leiser, R.
- Affiliations
- Justus-Liebig-Universität Gießen (DE)
- Loma Linda University (US)
- Corresponding author
- Krebsa, C.
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 1997-01
- Volume
- 18
- Issue
- 1
- Pages
- 43-51
- ISSN
- 0143-4004 (ISSN-L)
- OpenAlex
- W2037637848
- Cited by
- 71
- References
- 60
- Citations by year
- 2025: 2 · 2021: 4 · 2020: 2 · 2019: 1 · 2018: 2 · 2017: 2 · 2016: 2 · 2015: 5 · 2014: 1 · 2013: 3 · 2012: 2
- FWCI
- 2.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Placenta (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › High Altitude and Hypoxia
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
- Keywords
- placental vasculature, high altitude, hypoxemia, fetal sheep, corrosion casts, histomorphometry, capillary network, vascular branching, gestation
- MeSH terms
- Altitude, Animals, Capillaries, Female, Fetus, Microscopy, Electron, Scanning, Placenta, Pregnancy, Sheep, Corrosion Casting
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