Stereological evaluation of vascular adaptations in human placental villi to differing forms of hypoxic stress
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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In all high-altitude populations studied to date, there is increased villous vascularisation as a result of increased vasculogenesis and angiogenesis.
“In all high-altitude populations studied to date, there is increased villous vascularisation as a result of increased vasculogenesis and angiogenesis (7, 78, 176, 509, 532).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [78]
This is achieved through selective dilation of the capillary sinusoids at the vasculosyncytial membranes, a mechanism that increases placental diffusing capacity but has minimal effects on extracorporeal blood volume and the load on the fetal heart.
“This is achieved through selective dilation of the capillary sinusoids at the vasculosyncytial membranes (78), a mechanism that increases placental diffusing capacity but has minimal effects on extracorporeal blood volume and the load on the fetal heart.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [78]
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BackgroundAnalysis 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 · see citing works
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 · see citing works
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 · see citing works
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 · 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
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
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
“been reported to be impaired by reduced surface area, reduced capillary length density and/or greater trophoblast thickness ( 9 , 47).”
BackgroundMaternal 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 34 · see citing works
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 · see citing works
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 · see citing works
Wilsher, S. A., & Allen, W. R. T. (2006) · Equine Veterinary Journal · doi:10.2746/042516406x156497 · Cited by 32 · 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
“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.”
BackgroundMayhew, T. M. (2006) · Journal of Anatomy · doi:10.1111/j.1469-7580.2006.00566.x · Cited by 31 · see citing works
“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).”
BackgroundLi, 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 · see citing works
“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…”
BackgroundResultInfluentialDistinct 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 · 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
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 · see citing works
“The increased density and the number of capillaries as well as compensatory placental hypertrophy have been reported in anemic women [71,72].”
BackgroundEscudero, C., Puebla, C., Westermeier, F., & Sobrevía, L. (2009) · Current Vascular Pharmacology · doi:10.2174/157016109789043865 · Cited by 28 · see citing works
“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.”
BackgroundJiang, 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 · see citing works
“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].”
BackgroundEffects 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 · see citing works
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 20 · see citing works
Robertson, C. E., & Wilsterman, K. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.215350 · Cited by 20 · see citing works
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 · see citing works
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 17 · see citing works
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 15 · see citing works
“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.
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 1996-01
- Volume
- 17
- Issue
- 1
- Pages
- 49-55
- ISSN
- 0143-4004 (ISSN-L)
- 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
- Locations
- Placenta (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › 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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