Does hypercapillarization influence the branching pattern of terminal villi in the human placenta at high altitude?
Abstract
This study tests the hypothesis that exposure of the placenta to hypobaric hypoxia at altitude results in an altered branching pattern of the villous tree. Histological material from 20 term placentae delivered at altitudes over 3000 m was compared with matched controls from 500 m. Estimates of the mean star volume of intermediate and terminal villous domains were 1.40 x 10(6) microns3 (s.d. 0.63) in the high altitude group and 1.90 x 10(6) microns3 (s.d. 0.34) in the controls (F = 9.07, P < 0.005). The volume fraction of the villous tree occupied by trophoblastic bridges and syncytial knots was 8.1 per cent (s.d. 3.5) in the high altitude group and 3.2 per cent (s.d. 1.6) in the controls (F = 29.45, P < 0.0001). Previous studies have shown that the majority (80 per cent) of bridges are artefacts caused by the plane of section passing tangentially through the trophoblast layer at points of villous bending or branching. The results are, therefore, consistent with the hypothesis that peripheral villi are shorter, knob-like protrusions at high altitude, clustered more closely together. This modified branching pattern was confirmed by scanning electron microscopy. The change in architecture may be due to enhanced angiogenesis stimulated by the lower partial pressure of oxygen prevailing at high altitude.
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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 [7]
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 [7]
At high altitude, there is increased branching and reduced coiling of the fetal capillaries in the placenta with more densely packed capillary loops in the terminal villi responsible for gas exchange.
“At high altitude, there is increased branching and reduced coiling of the fetal capillaries in the placenta with more densely packed capillary loops in the terminal villi responsible for gas exchange (7,532).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [7]
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
Practical methods for biological morphometry
Weibel, E. R. (1979) · Academic Press eBooks · Cited by 1,502 · see citing works
Gundersen, H. J. G., & Jensen, E. B. V. (1985) · Journal of Microscopy · doi:10.1111/j.1365-2818.1985.tb02607.x · Cited by 492 · see citing works
Weibel, M. (1984) · Cited by 278 · 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
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-citationClassification of human placental villi
Kaufmann, P., Sen, D. K., & Schweikhart, G. (1979) · Cell and Tissue Research · doi:10.1007/bf00234852 · Cited by 147 · 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
Interpretation of syncytial sprouts and bridges in the human placenta
Cantle, S. J., Kaufmann, P., Luckhardt, M., & Schweikhart, G. (1987) · Placenta · doi:10.1016/0143-4004(87)90046-4 · Cited by 111 · see citing works
Angiogenesis and the placental environment
Wheeler, T., Elcock, C. L., & Anthony, F. W. (1995) · Placenta · doi:10.1016/0143-4004(95)90115-9 · Cited by 110 · see citing works
Three-Dimensional Representation of the Fetal Vessel System in the Human Placenta
Kaufmann, P., Luckhardt, M., & Leiser, R. (1988) · Springer eBooks · doi:10.1007/978-1-4615-8109-3_9 · Cited by 81 · see citing works
Cross-sectional features and three-dimensional structure of human placental Villi
Kaufmann, P., Luckhardt, M., Schweikhart, G., & Cantle, S. J. (1987) · Placenta · doi:10.1016/0143-4004(87)90047-6 · Cited by 80 · see citing works
Burton, G. J., Mayhew, T. M., & Robertson, L. A. (1989) · Placenta · doi:10.1016/0143-4004(89)90027-1 · Cited by 44 · see citing works
Self-citationStar volumes of villi and intervillous pores in placentae from low and high altitude pregnancies.
Lee, R., & Mayhew, T. M. (1995) · PubMed · Cited by 20 · see citing works
[Syncytial sprouts and intervillous bridges in human placenta (author's transl)].
Kustermann, W. (1981) · PubMed · Cited by 7 · see citing works
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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
Self-citationDevelopmental 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-citationHumans 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
Zamudio, S. (2003) · High Altitude Medicine & Biology · doi:10.1089/152702903322022785 · Cited by 161 · see citing works
Syncytial Knots (Tenney-Parker Changes) in the Human Placenta
Fogarty, N. M. E., Ferguson-Smith, A. C., & Burton, G. J. (2013) · The American Journal of Pathology · doi:10.1016/j.ajpath.2013.03.016 · Cited by 116 · 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
- Authors
- Alia, K. Z. M., Burton, G. J., Morad, N., & Ali, M. E.
- Affiliations
- King Saud University (SA)
- University of Cambridge (GB)
- Corresponding author
- Burton, G.J.
- ORCID
- Burton, G.J.
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 1996
- Volume
- 17
- Issue
- 8
- Pages
- 677-682
- ISSN
- 0143-4004 (ISSN-L)
- OpenAlex
- W2029315997
- Cited by
- 64
- References
- 15
- Citations by year
- 2026: 1 · 2025: 1 · 2022: 3 · 2021: 5 · 2018: 3 · 2017: 1 · 2016: 2 · 2015: 2 · 2013: 1 · 2012: 4
- FWCI
- 1.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Placenta (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- 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 › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- terminal villi, high altitude, hypobaric hypoxia, placental angiogenesis, syncytial knots, villous architecture, oxygen partial pressure, human placenta
- MeSH terms
- Adult, Altitude, Capillaries, Female, Humans, Microscopy, Electron, Scanning, Microvilli, Placenta, Pregnancy, Trophoblasts
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