Cited by 149Pregnancy and preeclampsia studiesHigh Altitude and HypoxiaNeonatal and fetal brain pathology

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Stereological evaluation of vascular adaptations in human placental villi to differing forms of hypoxic stress

Burton, G.J., Reshetnikova, O.S., Milovanov, A.P., Teleshova, O.V.·1996·Placenta

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Abstract

The aim was to determine whether the fetal vasculature of the human placenta adapts in a uniform manner to different forms of hypoxic stress. Stereological analyses were performed on the intermediate and terminal villi of placentae obtained from each of the following conditions; high altitude (up to 2800 m), maternal iron-deficiency anaemia and pre-eclampsia. These conditions were taken to represent hypoxic, anaemic and ischaemic hypoxia, respectively. In each situation, there was a trend for the volume fraction of the fetal capillaries to be higher than in the controls, although the differences were statistically significant only for the cases of hypoxic and anaemia hypoxia. This was due, in part, to capillaries being of larger diameter. Evidence for capillary proliferation was inconsistent. At high altitude there was a trend for the capillary length density to be raised, but there was no change in the ratio of capillary:villous length. In both maternal anaemia and pre-eclampsia the capillary length density remained constant, but the ratio of capillary:villous length was significantly raised in the former. These results suggest that dilatation of the capillary sinusoids, with accompanying thinning of the villous membrane, is the principal adaptation to hypoxia under the conditions studied.

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Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis
Shweiki, D., Itin, A., Soffer, D., & Keshet, E. (1992) · Nature · doi:10.1038/359843a0 · Cited by 4,617
Pathology of the placenta.
Fox, H., & Elston, C. W. (1978) · PubMed · Cited by 621
The impact of recent stereological advances on quantitative studies of the nervous system
Brændgaard, H., & Gundersen, H. J. G. (1986) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(86)90112-3 · Cited by 501
Localization of two angiogenic growth factors (PDECGF and VEGF) in human placentae throughout gestation
Jackson, M., Carney, E. W., Lye, S. J., & Ritchie, J. W. K. (1994) · Placenta · doi:10.1016/0143-4004(94)90002-7 · Cited by 179
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
Chorangiosis. An important placental sign of neonatal morbidity and mortality.
Altshuler, G. P. (1984) · PubMed · Cited by 153
Classification of human placental villi
Kaufmann, P., Sen, D. K., & Schweikhart, G. (1979) · Cell and Tissue Research · doi:10.1007/bf00234852 · Cited by 147
Effects of hypobaric hypoxia on the fetoplacental unit: The morphometric diffusing capacity of the villous membrane at high altitude
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
Self-citation
Methodological problems in placental morphometry: Apologia for the use of stereology based on sound sampling practice
Mayhew, T. M., & Burton, G. J. (1988) · Placenta · doi:10.1016/0143-4004(88)90001-x · Cited by 114
Self-citation
Morphometric studies on villi in human term placentae and the effects of altitude, ethnic grouping and sex of newborn
Jackson, M. R., Mayhew, T. M., & Haas, J. D. (1987) · Placenta · doi:10.1016/0143-4004(87)90077-4 · Cited by 112

Show all 24 references

Research works printed but not linked: 3

Karimu, 1994, Compliance of the human placental villous membrane at term; the concept of the feto-placental unit as an autoregulating gas exchange system, Trophoblast Research, 8, 541
Reshetnikova, 1994, Human placental chorangioma at high altitude, Journal of Anatomy, 185, 223
Reshetnikova, O. S., Burton, G. J., Milovanov, A. P. et al (in press) Increased incidence of placental chorangioma in high altitude pregnancies; hypobaric hypoxia as a possible aetiological factor. American Journal of Obstetrics and Gynecology.

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Background
Analysis of the Fetal Placental Vascular Tree by X-ray Micro-computed Tomography
Langheinrich, A., Wienhard, J., Vormann, S., Hau, B., Bohle, R. M., & Zygmunt, M. (2003) · Placenta · doi:10.1016/j.placenta.2003.08.010 · Cited by 42
Blood pressure and hypertensive disorders of pregnancy at high altitude: a systematic review and meta-analysis
Grant, I. D., Giussani, D. A., & Aiken, C. (2021) · American Journal of Obstetrics & Gynecology MFM · doi:10.1016/j.ajogmf.2021.100400 · Cited by 41
Disorders of placental villous maturation are present in one-third of cases with spontaneous preterm labor
Jaiman, S., Romero, R. J., Pacora, P., Erez, O., Jung, E., Tarca, A. L., Bhatti, G., Yeo, L., Kim, Y. M., Kim, C. J., et al. (2021) · Journal of Perinatal Medicine · doi:10.1515/jpm-2020-0138 · Cited by 41
Histomorphometric study of placental villi vascular volume in toxemia and diabetes
Maly, A., Goshen, G., Sela, J., Pinelis, A., Stark, M. M., & Maly, B. (2005) · Human Pathology · doi:10.1016/j.humpath.2005.07.021 · Cited by 39
Pregnancy at high altitude
Krampl, E. (2002) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2002.00738.x · Cited by 37
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
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 37
“been reported to be impaired by reduced surface area, reduced capillary length density and/or greater trophoblast thickness ( 9 , 47).”
Background
Maternal iron homeostasis: effect on placental development and function
Roberts, H., Bourque, S. L., & Renaud, S. J. (2020) · Reproduction · doi:10.1530/rep-20-0271 · Cited by 36
Functional Magnetic Resonance Imaging (Magnetization Transfer) and Stereological Analysis of Human Placentae in Normal Pregnancy and in Pre-eclampsia and Intrauterine Growth Restriction
Ong, S., Tyler, D. J., Moore, R. J., Gowland, P. A., Baker, P. N., Johnson, I. R., & Mayhew, T. M. (2003) · Placenta · doi:10.1016/j.placenta.2003.10.011 · Cited by 34
Pharmacological activation of peroxisome proliferator‐activated receptor γ (PPAR‐γ) protects against hypoxia‐associated fetal growth restriction
Lane, S. L., Dodson, R. B., Doyle, A. S., Park, H., Rathi, H., Matarrazo, C. J., MOORE, L. G., Lorca, R. A., Wolfson, G. H., & Julian, C. G. (2019) · The FASEB Journal · doi:10.1096/fj.201900214r · Cited by 31
Effects of a Streptococcus equi infection‐mediated nutritional insult during mid‐gestation in primiparous Thoroughbred fillies. Part 1: Placental and fetal development
Wilsher, S. A., & Allen, W. R. T. (2006) · Equine Veterinary Journal · doi:10.2746/042516406x156497 · Cited by 32
Spatial arrangement of fetal placental capillaries in terminal villi: a study using confocal microscopy
Jirkovská, M., Kubínová, L., Krekule, I., & HACH, P. (1998) · Anatomy and Embryology · doi:10.1007/s004290050136 · Cited by 32
“Baur 1977; Sala et al. 1980; Teasdale 1983, 1987; Feneley and Burton 1991; Mayhew et al. 1993, 1994; Jirkovska et al. 1994a; Burton et al. 1996; Luckhardt et al. 1996) but three-dimensional (3-D) relationships and the branching pattern of villous capillaries have not yet been fully elucidated.”
Background
Allometric studies on growth and development of the human placenta: growth of tissue compartments and diffusive conductances in relation to placental volume and fetal mass
Mayhew, T. M. (2006) · Journal of Anatomy · doi:10.1111/j.1469-7580.2006.00566.x · Cited by 31
“They are maintained in maternal anaemia and preeclampsia (Reshetnikova et al. 1995; Burton et al. 1996) and increased at high altitude (Mayhew et al. 1990; Reshetnikova et al. 1994) and during maternal diabetes (Mayhew et al. 1993b).”
Background
Preeclampsia Does Not Alter Vascular Growth and Expression of CD31 and Vascular Endothelial Cadherin in Human Placentas
Li, Y., Zhao, Y., Zou, Q., Zhang, K. X., Wu, Y., Zhou, C., Wang, K., & Zheng, J. J. (2014) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155414558063 · Cited by 29
“In particular, Burton et al. (1996) demonstrated that the placental capillary volume fraction, capillary surface density, and capillary length density were all similar between PE pregnancies and GA-matched (38– 40 weeks) controls, even though 20% of the PE placentas were collected from mild PE…”
BackgroundResultInfluential
Distinct roles of HIF1A in endothelial adaptations to physiological and ambient oxygen
Jiang, Y., Li, Y., Wang, K., Dai, C., Huang, S., Chen, D., & Zheng, J. J. (2014) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.04.008 · Cited by 30
Morphometric Assessment of the Oxygen Diffusion Conductance in Placentae from Pregnancies Complicated by Intra-uterine Growth Restriction
Ansari, T. (2003) · Placenta · doi:10.1016/s0143-4004(03)00044-4 · Cited by 29
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
Mild anemia during pregnancy upregulates placental vascularity development
Stangret, A., Skoda, M., Wnuk, A., Pyźlak, M., & Szukiewicz, D. (2017) · Medical Hypotheses · doi:10.1016/j.mehy.2017.03.007 · Cited by 29
“The increased density and the number of capillaries as well as compensatory placental hypertrophy have been reported in anemic women [71,72].”
Background
Potential Cell Signalling Mechanisms Involved in Differential Placental Angiogenesis in Mild and Severe Pre-Eclampsia
Escudero, C., Puebla, C., Westermeier, F., & Sobrevía, L. (2009) · Current Vascular Pharmacology · doi:10.2174/157016109789043865 · Cited by 28
“A reduction in the total surface and length of the placental capillary [85] or no changes [75, 86] had been detected in pre-eclamptic placenta.”
Background
Transcriptional and Functional Adaptations of Human Endothelial Cells to Physiological Chronic Low Oxygen1
Jiang, Y., Wang, K., Li, Y., Dai, C., Wang, P., Kendziorski, C. M., Chen, D., & Zheng, J. J. (2013) · Biology of Reproduction · doi:10.1095/biolreprod.113.108225 · Cited by 27
“For example, at high altitudes, where O2 tension is lower than at sea level, placental villous vascularization is greatly increased in European pregnant women compared with those at sea level [6, 7].”
Background
Effects of Developmental Hypoxia on the Vertebrate Cardiovascular System
Galli, G. L. J., Lock, M. C., Smith, K. L. M., Giussani, D. A., & Crossley, D. A. (2022) · Physiology · doi:10.1152/physiol.00022.2022 · Cited by 26
Feto-placental Unit: From Development to Function
Covarrubias, A. E., Aguilera-Olguín, M., Carrasco‐Wong, I., Pardo, F., Díaz-Astudillo, P., & Martín, S. S. (2023) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-32554-0_1 · Cited by 22
Developmental and reproductive physiology of small mammals at high altitude: challenges and evolutionary innovations
Robertson, C. E., & Wilsterman, K. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.215350 · Cited by 21
Fetal growth, high altitude, and evolutionary adaptation: a new perspective
Wilsterman, K., & Cheviron, Z. A. (2021) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00067.2021 · Cited by 19
Exposure to fine particulate matter 2.5 from wood combustion smoke causes vascular changes in placenta and reduce fetal size
Villarroel, F., Ponce, N., Gómez, F. A., Muñoz, C., Ramírez, E., Nualart, F., & Salinas, P. (2024) · Reproductive Toxicology · doi:10.1016/j.reprotox.2024.108610 · Cited by 19
Enhanced Cellular Responses and Distinct Gene Profiles in Human Fetoplacental Artery Endothelial Cells under Chronic Low Oxygen1
Jiang, Y., Wang, K., Li, Y., Dai, C., Wang, P., Kendziorski, C. M., Chen, D., & Zheng, J. J. (2013) · Biology of Reproduction · doi:10.1095/biolreprod.113.110551 · Cited by 16
“In contrast, many diseases associated with endothelial dysfunction such as preeclampsia and atherosclerosis-induced chronic ischemia are often accompanied by an even lower pO2 [10–13].”

Authors: Burton, G. J., Reshetnikova, O. S., Milovanov, A. P., & Teleshova, O. V.
Affiliations: University of Cambridge (GB)
Luhansk State Medical University (UA)
Corresponding author: Burton, G.J.
ORCID: Burton, G.J.
Reshetnikova, O.S.
Venue: Placenta
Publisher: Elsevier BV
Published: 1996-01
Volume: 17
Issue: 1
Pages: 49-55
ISSN: 0143-4004 (ISSN-L)
DOI: 10.1016/s0143-4004(05)80643-5
OpenAlex: W1967702415
Cited by: 149
References: 24
Citations by year: 2026: 3 · 2025: 1 · 2024: 5 · 2023: 4 · 2022: 2 · 2021: 6 · 2020: 6 · 2019: 3 · 2018: 5 · 2017: 3 · 2016: 6 · 2015: 2 · 2014: 5 · 2013: 5 · 2012: 7
FWCI: 8.65
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Placenta (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Physiology (medical) › High Altitude and Hypoxia
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
Keywords: placental villi, fetal vasculature, hypoxic stress, high altitude, preeclampsia, capillary density, capillary dilation, stereology
MeSH terms: Altitude, Hypoxia, Capillaries, Female, Fetus, Humans, Male, Placenta, Pre-Eclampsia, Pregnancy, Pregnancy Complications, Anemia, Iron-Deficiency

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Stereological evaluation of vascular adaptations in human placental villi to differing forms of hypoxic stress

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