The DOI matches its Crossref record; 24 of the 24 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
In the citing paper
“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]
Citations
Cites
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
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
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
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-citationMayhew, T. M., & Burton, G. J. (1988) · Placenta · doi:10.1016/0143-4004(88)90001-x · Cited by 114
Self-citationJackson, M. R., Mayhew, T. M., & Haas, J. D. (1987) · Placenta · doi:10.1016/0143-4004(87)90077-4 · Cited by 112
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.
Cited by
Sorted by citations
Items 101–148 of 148
Numerical criteria for the diagnosis of placental chorangiosis using CD34 immunostaining
Mutema, G. K., & Stanek, J. W. (1999) · Placenta · doi:10.1016/s0143-4004(99)80033-2 · Cited by 15
Tongpob, Y., & Wyrwoll, C. S. (2020) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174420000720 · Cited by 13
Crossey, P. A., Pillai, C. C., & MIELL, J. P. (2002) · Journal of Clinical Investigation · doi:10.1172/jci200210077 · Cited by 11
Bierens, J., Severens‐Rijvers, C., Hildebrand, S., van Zandvoort, M. A. M. J., Al‐Nasiry, S., & Kapsokalyvas, D. (2025) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2025.03.015 · Cited by 10
Zou, Q., Zhao, Y., Li, H., Wang, X. M., Liu, A., Zhong, X., Yan, Q., Li, Y., Zhou, C., & Zheng, J. J. (2018) · The Journal of Physiology · doi:10.1113/jp275677 · Cited by 9
“These low O2 levels are assumed to be important for normal endothelial function (Burton et al. 1996; Mayhew, 2003; Zamudio, 2007; Meschia, 2013), including gene expression and FGF2- and VEGFA-induced fetoplacental endothelial responses (Jiang et al. 2013a,b).”
BackgroundAltered 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
“Such compensatory mechanisms may have been initiated in SIDS-SGA, however they are insufficient to maintain birthweight at a level comparable to controls and previous studies demonstrate reduced birthweights despite physiological compensatory adjustments aimed at increasing diffusional exchange such as reduced trophob…”
ResultSTEREOLOGICAL STUDIES ON FETAL VASCULAR DEVELOPMENT IN HUMAN PLACENTAL VILLI
Mayhew, T. M. (2011) · Image Analysis & Stereology · doi:10.5566/ias.v22.p49-56 · Cited by 8
“These ratios (3-4 km/km) are consistent with earlier estimates (e.g. Burton et al., 1996; Mayhew, 2002b) and with an average of about two capillary loops per villus (Benirschke and Kaufmann, 2000).”
ResultHISTOLOGICAL ABNORMALITIES OF THE PLACENTA
Fox, H., & Sebire, N. J. (2007) · Elsevier eBooks · doi:10.1016/b978-1-4160-2592-4.50011-4 · Cited by 8
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
Kingdom, J. C., Macara, L., Krebs, C., Leiser, R., & Kaufmann, P. (1997) · Placenta · doi:10.1016/s0143-4004(97)80095-1 · Cited by 7
An endogenous aryl hydrocarbon receptor ligand induces preeclampsia‐like phenotypes in rats
Zhao, Y., Zhou, C., Zhang, S., Mishra, J. S., Li, H., Lei, W., Wang, K., Kumar, S., & Zheng, J. J. (2024) · The Journal of Physiology · doi:10.1113/jp287503 · Cited by 6
“Although it was previously believed that PE does not affect vascular growth in human placentas (Burton et al., 1996; Li, Zhao et al., 2015), more recent reports using the more comprehensive 3D imaging analysis demonstrate that PE reduces placental vascular growth (Hermans et al., 2023; Shen et al.,…”
Mertz, H., Mele, L., Spong, C. Y., Dudley, D. J., Wapner, R. J., Iams, J. D., Sorokin, Y., Peaceman, A. M., Leveno, K. J., Caritis, S. N., et al. (2011) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2011.02.021 · Cited by 5
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
Widdows, K. L. (2009) · Brunel University Research Archive (BURA) (Brunel University London) · Cited by 5
Gebremeskel, T., Mulu, A., Kumbi, S., & Ergete, W. (2020) · Ethiopian Journal of Health Sciences · doi:10.4314/ejhs.v30i5.18 · Cited by 4
“insufficiency and low birth weight babies (11).”
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
Self-citationMarković, S., Cerovac, A., Kunosić, S., Ramić, S., & Bečirović, E. (2019) · Medicinski Glasnik · doi:10.17392/1055-19 · Cited by 4
Variability of Placental Expression of Cyclin E Low Molecular Weight Variants1
Bukovský, A., Cekanova, M., Caudle, M. R., Wimalasena, J., Foster, J. S., KEENAN, J. A., & Elder, R. F. (2002) · Biology of Reproduction · doi:10.1095/biolreprod67.2.568 · Cited by 4
“Hence, the excessive compensatory dilatation of sinusoids appears to represent an ultimate adaptive mechanism to fetal hypoxia, as suggested by others [25].”
BackgroundInfluentialSchliefsteiner, C., Wadsack, C., & Allerkamp, H. H. (2024) · Comprehensive physiology · doi:10.1002/cphy.c230020 · Cited by 6
Ancestry dependent balancing selection of placental dysferlin at high-altitude
Gundling, W. E., Post, S., Illsley, N. P., Echalar, L., Zamudio, S., & Wildman, D. E. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1125972 · Cited by 3
“It is unsurprising, given dysferlin’s role in the muscle sarcolemma, that numerous pathogenic mutations in the dysferlin gene are linked to muscle wasting diseases known collectively as dysferlinopathies and attributable to failure of muscle repair mechanisms (Charnay et al., 2021).”
BackgroundIntrauterine Wachstumsretardierung (IUWR)
Schneider, H., & Schneider, K. T. M. (2004) · Springer eBooks · doi:10.1007/978-3-642-18574-8_28 · Cited by 3
Stereological analysis of terminal villi of the placentas of pregnant woman with sideropenic anemia
Lelić, M., Ramić, S., Žigić, Z., Bogdanovic, G., & Marković, S. (2014) · Biomolecules and Biomedicine · doi:10.17305/bjbms.2014.3.44 · Cited by 3
“Placental villi exposed to low oxygen partial pressure may show an increase of fetal capillaries, even there are no exact evidence of capillary proliferation and changes are result of capillary dilatation [32].”
BackgroundAspectos estereológicos dos vilos coriônicos da placenta de bovinos clonados
Lacerda, P. M. D. O. (2006) · doi:10.11606/d.10.2006.tde-09082007-104255 · Cited by 3
Gundling, W. E., Pantham, P., Illsley, N. P., Echalar, L., Zamudio, S., & Wildman, D. E. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/261974 · Cited by 3
The relationship between maternal anemia and electronic fetal monitoring patterns
Beermann, S. E., Watkins, V. Y., Frolova, A. I., Raghuraman, N., & Cahill, A. G. (2023) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2023.04.018 · Cited by 2
Placental Morphology and Morphometry: Is It a Prerequisite for Future Pathological Investigations?
Govender, N., Lazarus, L., Abel, T., & Naicker, T. (2022) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-13021-2_5 · Cited by 3
Disproportion fœto-placentaire à terme : physiologique ou pathologique
Lorain, P., Boujenah, J., Bricou, A., Benbara, A., & Carbillon, L. (2015) · Journal de gynécologie, obstétrique et biologie de la reproduction. Supplément/Journal de gynécologie obstétrique et biologie de la reproduction · doi:10.1016/j.jgyn.2015.06.021 · Cited by 2
Placental Functional Morphology
Burton, G. J. (2001) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4612-0213-4_15 · Cited by 2
Self-citationPlacental Vascular Morphogenesis: Introduction and Overview
Jones, D. S., & Smith, S. K. (2001) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4612-0213-4_14 · Cited by 2
Intrauterine Wachstumsrestriktion (IUWR)
Schneider, H., & Schneider, K. T. M. (2011) · Springer eBooks · doi:10.1007/978-3-642-12974-2_27 · Cited by 1
Plewka, A., Plewka, D., & Nowaczyk, G. (2012) · InTech eBooks · doi:10.5772/32336 · Cited by 1
“In general, the abnormalities are linked to degeneration of villi although they involve also interstitial fibrosis and swelling of sinusoids in the villi [30,31].”
BackgroundPlacental pathology clues for interdisciplinary clarification of fetal disease
Altshuler, G. P. (1999) · Placenta · doi:10.1016/s0143-4004(99)80040-x · Cited by 1
Kiran, N., Mudassar, S., & Adeel, B. (2018) · International Journal of Contemporary Medical Research [IJCMR] · doi:10.21276/ijcmr.2018.5.8.19 · Cited by 1
Intrauterine Wachstumsretardierung (IUGR)
Schneider, H., & Schneider, K. T. M. (2007) · Springer eBooks · doi:10.1007/978-3-540-33897-0_28 · Cited by 1
Intrauterine Wachstumsretardierung (IUWR)
Schneider, H., & Schneider, K. T. M. (2000) · Springer eBooks · doi:10.1007/978-3-642-98004-6_27 · Cited by 1
Zhao, Y., Zhou, C., Wei, Y., Zhang, S., Mishra, J. S., Li, H., Lei, W., Wang, K., Kumar, S., & Zheng, J. J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.20.572271 · Cited by 1
“However, as PE does not alter vascular growth in human placentas 35,36 , different mechanisms may govern PE and ITE-induced hypertension in rats.”
BackgroundClinical and pathophysiological aspects of intrahepatic cholestasis of pregnancy
Shemer, E. W., & Alanio, E. (2012) · Figshare
Placental histomorphology: a predictor of foetal outcome in multiparous women
Munjal, S., Puja, C., & Mahima, M. (2014) · International Journal of Medical Research & Health Sciences · doi:10.5958/j.2319-5886.3.2.073
Volkmer, A. K. (2010) · Univ. Duesseldorf: Duesseldorfer Dokumenten- und Publikationsserver
Study of histological changes in placenta of anaemic mothers
Bala, S. R. (2016) · Journal of Anatomical Society of India · doi:10.1016/j.jasi.2016.08.258
“Burton et al [2] that fetal vasculature of human placenta adapt in a uniform manner in different form of hypoxic stress like high altitude and maternal iron deficiency anaemia .”
Background27 Intrauterine Wachstumsrestriktion (IUWR)
Schneider, H., & Untersuchung, K. (2011)
Deda, L. (2010) · TSpace (University of Toronto)
Placental Changes in Anemia, Gestational Diabetes and Pregnancy Induced Hypertension
Potuganti, M., & Zambare, B. R. (2020) · Academia Anatomica International · doi:10.21276/aanat.2020.6.2.19
Mezdoud, A., Agli, A.-N., & Oulamara, H. (2021) · Nutrition Clinique et Métabolisme · doi:10.1016/j.nupar.2021.02.005
Sinou, N., Shihada, A., Samolis, Α., Sinou, N., Troupis, T. G., & Filippou, D. K. (2026) · Cureus · doi:10.7759/cureus.107004
“Overall, 3D analyses demonstrate that the human placenta is hierarchically organized, biomechanically sophisticated, and functionally efficient, with villous branching patterns that are both structurally conserved and adaptively responsive to intrauterine conditions [38].”
Arenas, G. A., Herrera, E. A., Krause, B. J., Giussani, D. A., Julian, C. G., MOORE, L. G., & Lorca, R. A. (2026) · Physiological Reviews · doi:10.1152/physrev.00003.2026 · Cited by 1
Mixed Vascular Malperfusion: A Hemodynamic Coupling Framework for Placental Vascular Injury
Keir, H. M., & Kim, C. F. (2026) · Pediatric and Developmental Pathology · doi:10.1177/10935266261477802
Metadata
- 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
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review