Effects of hypobaric hypoxia on the fetoplacental unit: The morphometric diffusing capacity of the villous membrane at high altitude
Abstract
Objective Our purpose was to determine whether the human placenta is able to adapt structurally to hypobaric hypoxia so as to increase its diffusing capacity.Study design Material from 10 normal term placentas collected at each of three altitudinal levels in Kirghizstan was analyzed stereologically. Data were compared by one-way analysis of variance.Results Within the overall sample group birth weight and placental weight remained constant. There were no differences in villous and capillary surface areas or capillary length, but capillary volume increased from 37.9 cm3 in controls (700 m) to 50.8 cm3 at high altitude (2200 to 2800 m). The harmonic mean thickness fell from 6.9 microns in controls to 4.8 microns at high altitude. Consequently, the morphometric diffusing capacity of the villous membrane for oxygen increased from 4.22 to 7.56 cm3.min-1.mm Hg-1 (F = 6.45, p < 0.05).Conclusions The placenta is capable of adapting to hypobaric hypoxia to increase its functional capacity for gaseous exchange. This is principally through a reduction in the thickness of the villous membrane.
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Under limiting conditions such as pregnancy at high altitude, changes in surface area or membrane thickness may be adaptive responses to facilitate exchange.
“However, under limiting conditions, such as pregnancy at high altitude, changes in surface area or membrane thickness may be considered adaptive responses to facilitate exchange (275, 369, 458).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [458]
Studies show no consistent effect of chronic hypoxia on placental weight or size, with increases, decreases and no change depending on the study and/or population.
“These show no consistent effect of chronic hypoxia on placental weight or size with increases, decreases and no change depending on the study and/or population.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [458]
There is thinning of the interhemal membrane in the human placenta at high altitude.
“In addition, there is thinning of the interhemal membrane in the human placenta at high altitude (276, 366, 458).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [458]
Cites
Fetal nutrition and cardiovascular disease in adult life
Barker, D. J. P., Godfrey, K. M., Gluckman, P. D., Harding, J. E., Owens, J. A., & Robinson, J. S. (1993) · The Lancet · doi:10.1016/0140-6736(93)91224-a · Cited by 2,753 · see citing works
Stereological Methods. Practical methods for biological morphometry
Weibel, E. R. (1979) · Academic Press eBooks · Cited by 2,010 · see citing works
Fetal and placental size and risk of hypertension in adult life.
Barker, D. J., Bull, A. R., Osmond, C., & Simmonds, S. J. (1990) · BMJ · doi:10.1136/bmj.301.6746.259 · Cited by 1,728 · see citing works
Practical methods for biological morphometry
Weibel, E. R. (1979) · Academic Press eBooks · Cited by 1,502 · see citing works
Fetal and infant origins of adult disease
Barker, D. J. P. (2001) · Monatsschrift Kinderheilkunde · doi:10.1007/s001120170002 · Cited by 1,042 · see citing works
Fetal and Infant Origins of Adult Disease.
Artman, M. (1993) · Cardiovascular Research · doi:10.1093/cvr/27.6.1137a · Cited by 393 · see citing works
Morphometric estimation of pulmonary diffusion capacity
Weibel, E. R. (1970) · Respiration Physiology · doi:10.1016/0034-5687(70)90102-7 · Cited by 378 · see citing works
Morphometric estimation of pulmonary diffusion capacity
Burri, P. H., & Weibel, E. R. (1971) · Respiration Physiology · doi:10.1016/0034-5687(71)90028-4 · Cited by 192 · see citing works
The Biology of High-Altitude Peoples
Eveleth, P. B., & Baker, P. T. (1979) · Man · doi:10.2307/2801878 · Cited by 176 · see citing works
Altitude, Low Birth Weight, and Infant Mortality in Colorado
Unger, C. A. (1988) · JAMA · doi:10.1001/jama.1988.03720230037027 · Cited by 146 · see citing works
The placenta and the newborn infant at high altitudes
Kruger, H., & Arias‐Stella, J. (1970) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(70)90045-1 · Cited by 135 · see citing works
Fetal and placental size and risk of hypertension in adult life
Barker, D. J. P., Bull, A. R., Osmond, C., & Simmonds, S. (1991) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(91)90104-d · Cited by 128 · see citing works
Quantitative Studies of Human Placenta I.
Laga, E. M., Driscoll, S. G., & Munro, H. N. (2009) · Biology of the Neonate · doi:10.1159/000240605 · Cited by 117 · see citing works
Mayhew, T. M., & Burton, G. J. (1988) · Placenta · doi:10.1016/0143-4004(88)90001-x · Cited by 114 · see citing works
Self-citationBurggren, W. W., & Mwalukoma, A. (1983) · Journal of Experimental Biology · doi:10.1242/jeb.105.1.191 · Cited by 89 · see citing works
Effects of High Altitude on Human Birth
McClung, J. (1969) · Harvard University Press eBooks · doi:10.4159/harvard.9780674428614 · Cited by 83 · see citing works
Altitude-aggravated illness: Examples from pregnancy and prenatal life
MOORE, L. G. (1987) · Annals of Emergency Medicine · doi:10.1016/s0196-0644(87)80742-4 · Cited by 79 · 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
Feneley, M. R., & Burton, G. J. (1991) · Placenta · doi:10.1016/0143-4004(91)90017-a · Cited by 47 · see citing works
Self-citationBurton, G. J., & Palmer, M. E. (1992) · Journal of Experimental Zoology · doi:10.1002/jez.1402620309 · Cited by 45 · see citing works
Self-citationQuantitative Studies of Human Placenta II.
Laga, E. M., Driscoll, S. G., & Munro, H. N. (2009) · Biology of the Neonate · doi:10.1159/000240606 · Cited by 39 · see citing works
Burton, G. J., & Palmer, M. E. (1988) · Placenta · doi:10.1016/0143-4004(88)90040-9 · Cited by 31 · see citing works
Self-citationSystemic vascular reactivity during high-altitude pregnancy
Harrison, G. L., & MOORE, L. G. (1990) · Journal of Applied Physiology · doi:10.1152/jappl.1990.69.1.201 · Cited by 26 · see citing works
Comparative Morphometry of the Human Placenta at High Altitude and at Sea Level
Chabes, A., PEREDA, J., Hyams, L., BARRIENTOS, N., Pérez, J. O., CAMPOS, L., MONROE, A., & MAYORGA, A. (1968) · Obstetrics and Gynecology · doi:10.1097/00006250-196802000-00005 · Cited by 25 · see citing works
Expercise in pregnancy and placental development: A stereological analysis
Jackson, M., Ritchie, J. W. K., & Clapp, J. (1993) · Placenta · doi:10.1016/s0143-4004(05)80528-4 · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 26 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The Placenta: A Multifaceted, Transient Organ
Burton, G. J., & Fowden, A. L. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0066 · Cited by 833 · see citing works
Self-citationPlacental 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
Self-citationOxygen and placental villous development: Origins of fetal hypoxia
Kingdom, J. C., & Kaufmann, P. (1997) · Placenta · doi:10.1016/s0143-4004(97)90000-x · Cited by 581 · see citing works
Jansson, T., & Powell, T. L. (2007) · Clinical Science · doi:10.1042/cs20060339 · Cited by 542 · 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
Developmental Dynamics of the Definitive Mouse Placenta Assessed by Stereology1
Coan, P. M., Ferguson-Smith, A. C., & Burton, G. J. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.024166 · Cited by 296 · see citing works
Self-citationIlekis, J. V., Tsilou, E. T., Fisher, S. J., Abrahams, V. M., Soares, M. J., Cross, J. C., Zamudio, S., Illsley, N. P., Myatt, L., Colvis, C. M., et al. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.03.001 · Cited by 291 · see citing works
Hypoxia and Reoxygenation: a Possible Mechanism for Placental Oxidative Stress in Preeclampsia
Hung, T., & Burton, G. J. (2006) · Taiwanese Journal of Obstetrics and Gynecology · doi:10.1016/s1028-4559(09)60224-2 · Cited by 289 · see citing works
Self-citationOxygen, the Janus gas; its effects on human placental development and function
Burton, G. J. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.00978.x · Cited by 281 · see citing works
Self-citationThe Placenta and Intrauterine Programming
Fowden, A. L., Forhead, A. J., Coan, P. M., & Burton, G. J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01663.x · Cited by 267 · see citing works
Self-citationPlacental Adaptations in Growth Restriction
Zhang, S., Regnault, T. R. H., Barker, P., Botting, K. J., McMillen, I. C., McMillan, C., Roberts, C. T., & Morrison, J. L. (2015) · Nutrients · doi:10.3390/nu7010360 · Cited by 261 · see citing works
Humans at high altitude: Hypoxia and fetal growth
Moore, L. G., Charles, S. M., & Julian, C. G. (2011) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2011.04.017 · Cited by 251 · see citing works
Effects of Altitude versus Economic Status on Birth Weight and Body Shape at Birth
Giussani, D. A., Phillips, P. S., Anstee, S., & Barker, D. J. P. (2001) · Pediatric Research · doi:10.1203/00006450-200104000-00009 · Cited by 230 · see citing works
Sandovici, I., Hoelle, K., Angiolini, E., & Constância, M. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.03.017 · Cited by 224 · see citing works
Hung, T., Jones, D. S., Skepper, J. N., & Burton, G. J. (2004) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63192-6 · Cited by 209 · see citing works
Self-citationGestational Hypoxia and Developmental Plasticity
Ducsay, C. A., Goyal, R., Pearce, W. J., Wilson, S. M., Hu, X., & Zhang, L. (2018) · Physiological Reviews · doi:10.1152/physrev.00043.2017 · Cited by 203 · see citing works
Braun, T., Challis, J. R., Newnham, J. P., & Sloboda, D. M. (2013) · Endocrine Reviews · doi:10.1210/er.2013-1012 · Cited by 196 · see citing works
Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast, in vitro
Alsat, E., Wyplosz, P., Malassiné, A., Guibourdenche, J., Porquet, D., Nessmann, C., & Evain‐Brion, D. (1996) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(199608)168:2 · Cited by 177 · see citing works
The Impact of Hypoxia in Early Pregnancy on Placental Cells
Zhao, H. F., Wong, R. J., & Stevenson, D. K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22189675 · Cited by 183 · see citing works
Crossey, P. A., Pillai, C. C., & MIELL, J. P. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0210077 · Cited by 170 · see citing works
Zamudio, S. (2003) · High Altitude Medicine & Biology · doi:10.1089/152702903322022785 · Cited by 161 · 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
Li, A., Prasad, A., Mincemoyer, R., Satorius, C. L., Epstein, N., Finkel, T., & Quyyumi, A. A. (1999) · American Journal of Medical Genetics · doi:10.1002/(sici)1096-8628(19990903)86:1 · Cited by 66 · see citing works
Burton, 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
Self-citationAnatomy and Genesis of the Placenta
Burton, G. J., Kaufmann, P., & Huppertz, B. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50010-5 · Cited by 146 · see citing works
Self-citationBush, P. G., Mayhew, T. M., Abramovich, D. R., Aggett, P. J., Burke, M. D., & Page, K. (2000) · Placenta · doi:10.1053/plac.1999.0470 · Cited by 138 · see citing works
Stereologic examination of placentas from mothers who smoke during pregnancy
Larsen, L. G., Clausen, H. V., & Jönsson, L. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.120481 · Cited by 136 · see citing works
Crossey, P. A., Pillai, C. C., & MIELL, J. P. (2002) · Journal of Clinical Investigation · doi:10.1172/jci10077 · Cited by 133 · see citing works
Uterine artery blood flow, fetal hypoxia and fetal growth
Browne, V. A., Julian, C. G., Toledo-Jaldin, L., Cioffi-Ragan, D., Vargas, E., & Moore, L. G. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0068 · Cited by 127 · see citing works
Hypoxia: Adapting to High Altitude by Mutating <i>EPAS-1</i> , the Gene Encoding HIF-2α
Tissot van Patot, M. C., & Gassmann, M. (2011) · High Altitude Medicine & Biology · doi:10.1089/ham.2010.1099 · Cited by 119 · see citing works
Roh, C., Budhraja, V., Kim, H.-S., Nelson, D. M., & Sadovsky, Y. (2004) · Placenta · doi:10.1016/j.placenta.2004.06.013 · Cited by 113 · see citing works
Yung, H. W., Cox, M., van Patot, M. T., & Burton, G. J. (2012) · The FASEB Journal · doi:10.1096/fj.11-190082 · Cited by 112 · see citing works
Self-citationStereology and the Placenta: Where's the Point? – A Review
Mayhew, T. M. (2006) · Placenta · doi:10.1016/j.placenta.2005.11.006 · Cited by 110 · see citing works
Ascorbate prevents placental oxidative stress and enhances birth weight in hypoxic pregnancy in rats
Richter, H. G., Camm, E. J., Modi, B., Naeem, F., Cross, C. M., Cindrová‐Davies, T., Spasic‐Boskovic, O., Dunster, C., Mudway, I., Kelly, F. J., et al. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.226340 · Cited by 106 · see citing works
Self-citationMaternal Cigarette Smoking and Oxygen Diffusion Across the Placenta
Bush, P. G., Mayhew, T. M., Abramovich, D. R., Aggett, P. J., Burke, M. D., & Page, K. (2000) · Placenta · doi:10.1053/plac.2000.0571 · Cited by 83 · 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
Reshetnikova, O. S., Burton, G. J., & Васильевна, Т. О. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)90330-5 · Cited by 82 · see citing works
Self-citationMayhew, T. M. (2003) · Placenta · doi:10.1053/plac.2002.0895 · Cited by 75 · see citing works
Krebsa, C., Longob, L. D., & Leiser, R. (1997) · Placenta · doi:10.1016/s0143-4004(97)90070-9 · Cited by 71 · see citing works
Matheson, H., Veerbeek, J. H. W., Charnock‐Jones, D. S., Burton, G. J., & Yung, H. W. (2016) · The Journal of Physiology · doi:10.1113/jp271073 · Cited by 71 · see citing works
Self-citationPlacental Villus Morphology in Relation to Maternal Hypoxia at High Altitude
Espinoza, J., Sebire, N. J., McAuliffe, F., Krampl, E., & Nicolaides, K. H. (2001) · Placenta · doi:10.1053/plac.2001.0696 · Cited by 67 · see citing works
Remodelling of Uteroplacental Arteries is Decreased in High Altitude Placentae
Tissot van Patot, M., Grilli, A., Chapman, P., Broad, E., Tyson, W., Heller, D. S., Zwerdlinger, L., & Zamudio, S. (2003) · Placenta · doi:10.1053/plac.2002.0899 · Cited by 67 · 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-citationPlacental 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
Zhang, E., Burton, G. J., Smith, S. K., & Jones, D. S. (2002) · Placenta · doi:10.1053/plac.2002.0856 · Cited by 67 · see citing works
Self-citationThree-dimensional modeling of human placental terminal villi
Mayo, R. P., Jones, D. S., Burton, G. J., & Oyen, M. L. (2016) · Placenta · doi:10.1016/j.placenta.2016.05.001 · Cited by 64 · see citing works
Self-citationMayhew, T. M. (1996) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/0301-2115(96)02486-4 · Cited by 64 · see citing works
Fetoplacental oxygen homeostasis in pregnancies with maternal diabetes mellitus and obesity
Desoyé, G., & Carter, A. M. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00717-z · Cited by 59 · see citing works
Burton, G. J., & Hung, T. (2003) · Fetal and Maternal Medicine Review · doi:10.1017/s0965539503001049 · Cited by 52 · see citing works
Self-citationGene 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
Role of the Placenta in Perinatal Pathology (Revisited)
Altshuler, G. P. (1996) · Pediatric Pathology & Laboratory Medicine · doi:10.1080/15513819609169284 · Cited by 51 · see citing works
Full-term birth weight and placental morphology at high and low altitude
Khalid, M. E. M., Ali, M. E., & Ali, K. Z. M. (1997) · International Journal of Gynecology & Obstetrics · doi:10.1016/s0020-7292(97)00067-2 · Cited by 51 · 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
Self-citationNatale, B. V., Mehta, P., Vu, P., Schweitzer, C. L., Gustin, K., Kotadia, R., & Natale, D. R. C. (2018) · Scientific Reports · doi:10.1038/s41598-018-35606-x · Cited by 49 · see citing works
Mayhew, T. M. (1998) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(98)00154-7 · Cited by 46 · see citing works
Maternal anemia results in increased proliferation in human placental villi
Kosanke, G., Kadyrov, M., Korr, H., & Kaufmann, P. (1998) · Placenta · doi:10.1016/s0143-4004(98)80024-6 · Cited by 46 · see citing works
Soluble flt‐1 and the angiopoietins in the development and regulation of placental vasculature*
Jones, D. S. (2002) · Journal of Anatomy · doi:10.1046/j.1469-7580.2002.00063.x · Cited by 46 · see citing works
Chronic Hypoxia In Vivo Reduces Placental Oxidative Stress
Zamudio, S., Kovalenko, O., Vanderlelie, J. J., Illsley, N. P., Heller, D. S., Belliappa, S., & Perkins, A. V. (2007) · Placenta · doi:10.1016/j.placenta.2006.11.010 · Cited by 44 · see citing works
van Patot, M. C. T., Valdez, M., Becky, V., Cindrová‐Davies, T., Johns, J., Zwerdling, L., Jauniaux, E. R. M., & Burton, G. J. (2009) · Placenta · doi:10.1016/j.placenta.2009.04.002 · Cited by 42 · see citing works
Self-citationAli, K. Z. M. (1997) · Placenta · doi:10.1016/s0143-4004(97)80046-x · Cited by 42 · see citing works
Humerus varus deformity in Roman period burials from Kellis 2, Dakhleh, Egypt
Molto, J. E. (2000) · American Journal of Physical Anthropology · doi:10.1002/1096-8644(200009)113:1 · Cited by 40 · see citing works
Xiang, Y., Guo, L., Li, H., Chen, X., & Tong, X. (2011) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2011.601367 · Cited by 40 · see citing works
Soma, H., Hata, T., Oguro, T., Fujita, K., Kudo, M., & Vaidya, U. (2005) · Medical Molecular Morphology · doi:10.1007/s00795-004-0259-y · Cited by 37 · see citing works
Krampl, E. (2002) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2002.00738.x · Cited by 37 · see citing works
Hypoxia and Placental Remodelling
Cartwright, J. E., Keogh, R. J., & van Patot, M. C. T. (2007) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-75434-5_9 · Cited by 36 · see citing works
Maternal uterine artery Doppler studies at high altitude and sea level
Krampl, E., Dorado, J. E., LEES, C. C., Moscoso, G. J., Bland, M., & Campbell, S. C. (2001) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.0960-7692.2001.00579.x · Cited by 36 · see citing works
Trophoblast function in normal and preeclamptic pregnancy
Cross, J. C. (1996) · Fetal and Maternal Medicine Review · doi:10.1017/s0965539500001492 · Cited by 34 · see citing works
Mayhew, T. M. (2006) · Journal of Anatomy · doi:10.1111/j.1469-7580.2006.00566.x · Cited by 31 · see citing works
Fetal Doppler velocimetry at high altitude
Krampl, E., Lees, C. C., Bland, J. M., Dorado, J. E., Moscoso, G. J., & Campbell, S. C. (2001) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.0960-7692.2001.00542.x · Cited by 31 · see citing works
Ansari, T. (2003) · Placenta · doi:10.1016/s0143-4004(03)00044-4 · Cited by 29 · see citing works
Mayhew, T. M., Bowles, C., & Yücel, F. (2002) · Placenta · doi:10.1053/plac.2001.0775 · Cited by 28 · see citing works
The origin of pre-eclampsia: From decidual “hyperoxia” to late hypoxia
Tranquilli, A. L., & Landi, B. (2010) · Medical Hypotheses · doi:10.1016/j.mehy.2010.01.024 · Cited by 28 · see citing works
Lane, S. L., Doyle, A. S., Bales, E. S., Lorca, R. A., Julian, C. G., & MOORE, L. G. (2019) · Biology of Reproduction · doi:10.1093/biolre/ioz208 · Cited by 23 · see citing works
Cause of fetal growth restriction during high-altitude pregnancy
Brown, E. R., & Giussani, D. A. (2024) · iScience · doi:10.1016/j.isci.2024.109702 · Cited by 21 · see citing works
Placental oxygen transfer and the oxygen supply to the fetus
Carter, A. M. (1999) · Fetal and Maternal Medicine Review · doi:10.1017/s0965539599000352 · Cited by 19 · see citing works
The morphometry of materno–fetal oxygen exchange barrier in a baboon model of obesity
Samson, J. E., Mari, G., Dick, E. J., Hubbard, G. B., Ferry, R. J., & Schlabritz‐Loutsevitch, N. (2011) · Placenta · doi:10.1016/j.placenta.2011.07.083 · Cited by 17 · see citing works
A Prospective Study of Villous Capillary Lesions in Complicated Pregnancies
Srinivasan, A. P., Omprakash, B. O. P., Lavanya, K., Murugesan, P. S., & Kandaswamy, S. (2014) · Journal of Pregnancy · doi:10.1155/2014/193925 · Cited by 17 · see citing works
Placental angiogenesis: the role of the VEGF family of proteins
Clark, D. E., & Jones, D. S. (1998) · Angiogenesis · doi:10.1023/a:1009200824934 · Cited by 17 · see citing works
Mayhew, T. M. (2012) · Annals of Anatomy - Anatomischer Anzeiger · doi:10.1016/j.aanat.2012.08.002 · Cited by 17 · see citing works
Placental Adaptation to Hypoxia: The Case of High-Altitude Pregnancies
Ahrens, S., & Singer, D. (2025) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph22020214 · Cited by 18 · see citing works
Development of the Human Placental Villus
Aplin, J., Lewis, R. M., & Jones, C. J. P. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.99857-x · Cited by 15 · see citing works
Wee, L., Sebire, N. J., Bhundia, J., Sullivan, M. H. F., & Fisk, N. M. (2005) · Placenta · doi:10.1016/j.placenta.2005.02.020 · Cited by 15 · see citing works
Placental Gas Exchange and the Oxygen Supply to the Fetus
Carter, A. M. (2015) · Comprehensive physiology · doi:10.1002/j.2040-4603.2015.tb00648.x · Cited by 11 · see citing works
Aksoy, A. N., Batmaz, G., Dane, B., Kucur, S. K., & Gözükara, İ. (2015) · Journal of the Turkish-German Gynecological Association · doi:10.5152/jtgga.2015.15134 · Cited by 11 · see citing works
Global population variation in placental size and structure: Evidence from Cebu, Philippines
Rutherford, J. N., deMartelly, V. A., Ragsdale, H. B., Avila, J. L., Lee, N. R., & Kuzawa, C. W. (2019) · Placenta · doi:10.1016/j.placenta.2019.08.076 · Cited by 11 · see citing works
Clinical Care in Extreme Environments: At High and Low Pressure and in Space
Moon, R. E., & Camporesi, E. M. (2010) · Elsevier eBooks · doi:10.1016/b978-0-443-06959-8.00080-7 · Cited by 11 · see citing works
Crossey, P. A., Pillai, C. C., & MIELL, J. P. (2002) · Journal of Clinical Investigation · doi:10.1172/jci200210077 · Cited by 11 · see citing works
Benign Tumors and Chorangiosis
Benirschke, K., Burton, G. J., & Baergen, R. N. (2012) · Springer eBooks · doi:10.1007/978-3-642-23941-0_24 · Cited by 10 · see citing works
Self-citationHistopathological Approach to Villous Alterations
Benirschke, K., Burton, G. J., & Baergen, R. N. (2012) · Springer eBooks · doi:10.1007/978-3-642-23941-0_14 · Cited by 10 · see citing works
Self-citationBenirschke, K., & Kaufmann, P. (2000) · Springer eBooks · doi:10.1007/978-1-4757-4199-5_24 · Cited by 10 · see citing works
Uterine blood flow as a determinant of fetoplacental development
Moore, L. G. (2010) · The Placenta and Human Developmental Programming · doi:10.1017/cbo9780511933806.012 · Cited by 9 · see citing works
Ali, K. Z. M., Burton, G. J., Al-Binali, A. M., Eskandar, M. A., El-Mekki, A. A., Moosa, R. A., Abd-Alla, S. A., Salih, A. G. A., Sideeg, A. M., & Mahfouz, A. A. (2012) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2012.667462 · Cited by 10 · see citing works
Self-citationHistomorphometric parameters of normal full term placenta of Sudanese women
Abdalla, A. M., Tingari, M. D., & Abdalla, M. A. (2016) · Heliyon · doi:10.1016/j.heliyon.2016.e00135 · Cited by 9 · see citing works
Myres, J. E., Malan, M., Shumway, J. B., Rowe, M. J., Amon, E., & Woodward, S. R. (2000) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2000.107331 · Cited by 9 · see citing works
Altered placental development in pregnancies resulting in sudden infant death syndrome (SIDS)
Widdows, K. L., O'Malley, A., O'Neill, B., Kingdom, J. C., Gillan, J., & Ansari, T. (2012) · Early Human Development · doi:10.1016/j.earlhumdev.2012.05.006 · Cited by 8 · 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
Aplin, J., & Jones, C. J. P. (2008) · Reproductive medicine and assisted reproductive techniques series · doi:10.3109/9780203091500.030 · Cited by 8 · see citing works
Kingdom, J. C., Macara, L., Krebs, C., Leiser, R., & Kaufmann, P. (1997) · Placenta · doi:10.1016/s0143-4004(97)80095-1 · Cited by 7 · see citing works
Kuzawa, C. W. (1998) · doi:10.1002/(sici)1096-8644(1998)107:27+
- Authors
- Reshetnikova, O. S., Burton, G. J., & Milovanov, A. P.
- Affiliations
- Luhansk State Medical University (UA)
- University of Cambridge (GB)
- Corresponding author
- Burton, Graham J.
- Venue
- American Journal of Obstetrics and Gynecology
- Publisher
- Elsevier BV
- Published
- 1994-12
- Volume
- 171
- Issue
- 6
- Pages
- 1560-1565
- ISSN
- 0002-9378 (ISSN-L)
- OpenAlex
- W1998471670
- Cited by
- 127
- References
- 26
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 1 · 2023: 1 · 2022: 1 · 2021: 5 · 2020: 2 · 2019: 2 · 2018: 4 · 2016: 4 · 2015: 9 · 2014: 1 · 2013: 3 · 2012: 11
- FWCI
- 2.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Obstetrics and Gynecology (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
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- hypobaric hypoxia, high altitude, placenta, fetoplacental unit, diffusing capacity for carbon monoxide, placental adaptation, gas exchange, capillary volume, stereology, term placenta
- MeSH terms
- Altitude, Hypoxia, Atmospheric Pressure, Birth Weight, Capillaries, Diffusion, Female, Fetus, Humans, Microvilli, Placenta, Pregnancy
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