Cited by 1,057Pregnancy and preeclampsia studiesReproductive System and PregnancyNitric Oxide and Endothelin Effects

Onset of Maternal Arterial Blood Flow and Placental Oxidative Stress

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Jauniaux, Eric, Watson, Adrian L., Hempstock, Joanne, Bao, Yi-Ping, Skepper, Jeremy N., Burton, Graham J.·2000·The American Journal of Pathology

Abstract

The aim was to measure changes in the oxygen tension within the human placenta associated with onset of the maternal arterial circulation at the end of the first trimester of pregnancy, and the impact on placental tissues. Using a multiparameter probe we established that the oxygen tension rises steeply from <20 mmHg at 8 weeks of gestation to >50 mmHg at 12 weeks. This rise coincides with morphological changes in the uterine arteries that allow free flow of maternal blood into the placenta, and is associated with increases in the mRNA concentrations and activities of the antioxidant enzymes catalase, glutathione peroxidase, and manganese and copper/zinc superoxide dismutase within placental tissues. Between 8 to 9 weeks there is a sharp peak of expression of the inducible form of heat shock protein 70, formation of nitrotyrosine residues, and derangement of the mitochondrial cristae within the syncytiotrophoblast. We conclude that a burst of oxidative stress occurs in the normal placenta as the maternal circulation is established. We speculate that this may serve a physiological role in stimulating normal placental differentiation, but may also be a factor in the pathogenesis of pre-eclampsia and early pregnancy failure if antioxidant defenses are depleted.

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Crossref · 10.1016/s0002-9440(10)64849-3

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  • Higher intensity of oxidative stress can have adverse effects on the developing embryo and can lead to embryo fragmentation.

    “Higher intensity of oxidative stress can have adverse effects on the developing embryo, and can lead to embryo fragmentation (Jauniaux et al., 2000).”

    From Iron, Oxidative Stress and Health (2012) · cites this paper as Jauniaux et al., 2000

    The Discussion (page unavailable in our copy) says excessive placental oxidative stress may cause trophoblastic degeneration and, if severe, pregnancy failure. This supports the possibility of harm in early pregnancy, but the paper does not say oxidative stress leads to embryo fragmentation. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • In early gestation, the syncytiotrophoblast has low concentrations of antioxidant enzymes compared to other villous tissues, making it susceptible to oxidative stress.

    “During early gestation, the syncytiotrophoblast has low concentrations of antioxidant enzymes compared to other villous tissues, making it susceptible to oxidative stress (Jauniaux et al., 2000).”

    From Iron, Oxidative Stress and Health (2012) · cites this paper as Jauniaux et al., 2000

  • Placental metabolism is heavily glycolytic in early pregnancy due to the prevailing low oxygen concentration.

    “Placental metabolism is heavily glycolytic in early pregnancy due to the prevailing low oxygen concentration (286).”

    From Placental Origins of Chronic Disease (2016) · cites this paper as [286]

  • The intraplacental oxygen concentration of about 2.5% during the first trimester exceeds the evolutionary conserved range of maximal HIF activity of 0.5-2.0% oxygen.

    “In addition, the intraplacental oxygen concentration of ~2.5% during the first trimester exceeds the evolutionary conserved range of maximal HIF activity of 0.5 -2.0% oxygen (225, 286).”

    From Placental Origins of Chronic Disease (2016) · cites this paper as [286]

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Research works printed but not linked: 4

  1. Kurjak A, Kupesic S, Hafner T, Kos M, Kostovic-Knezevic L, Grbesa D: Conflicting data on intervillous circulation in early pregnancy. J Perinat Med 1997, 25:225-236
  2. Harris JWS, Ramsey EM: The morphology of human uteroplacental vasculature. Contrib Embryol 1966, 38:43-58
  3. Melendez JA, Baglioni C: Differential induction and decay of manga- nese superoxide-dismutase messenger-RNAs. Free Radic Biol Med 1993, 14:601-608
  4. Watson AL, Skepper JN, Jauniaux E, Burton GJ: Reducing oxidative stress effects in early human placental villi during in vitro culture. Placenta 1999, 20:A69

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Authors
Jauniaux, E., Watson, A. L., Hempstock, J., Bao, Y.-P., Skepper, J. N., & Burton, G. J.
Affiliations
  • University College London (GB)
  • University of Cambridge (GB)
Corresponding author
Burton, Graham J.
Venue
The American Journal of Pathology
Publisher
Elsevier BV
Published
2000-12
Volume
157
Issue
6
Pages
2111-2122
ISSN
0002-9440 (ISSN-L)
OpenAlex
W171819190
Cited by
1,057
References
49
Citations by year
2026: 22 · 2025: 34 · 2024: 43 · 2023: 44 · 2022: 57 · 2021: 67 · 2020: 50 · 2019: 48 · 2018: 57 · 2017: 44 · 2016: 39 · 2015: 40 · 2014: 51 · 2013: 48 · 2012: 45
FWCI
22.61
Type
journal article
Language
en
Open access
Locations
  • American Journal Of Pathology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Wellcome Trust
  • Directorate for Biological Sciences
Topics
  • Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
  • Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
  • Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Keywords
placental oxidative stress, first trimester, antioxidant enzymes, catalase, glutathione peroxidase, superoxide dismutase, HSP70, nitrotyrosine, syncytiotrophoblast, mitochondrial cristae, preeclampsia, early pregnancy failure, placental differentiation
MeSH terms
Abortion, Spontaneous, Arteries, Drug Residues, Female, Humans, Mitochondria, Oxidoreductases, Oxygen, Partial Pressure, Placenta, Pregnancy, Pregnancy Trimester, First, Regional Blood Flow, RNA, Messenger, Tyrosine, Oxidative Stress, HSP70 Heat-Shock Proteins

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