CoChat
Sign Up
Cited by 112Air Quality and Health ImpactsHealth, Environment, Cognitive AgingEnvironmental Justice and Health Disparities

Placental Nitrosative Stress and Exposure to Ambient Air Pollution During Gestation: A Population Study

Saenen, Nelly D., Vrijens, Karen, Janssen, Bram G., Madhloum, Narjes, Peusens, Martien, Gyselaers, Wilfried, Vanpoucke, Charlotte, Lefebvre, Wouter +2 more·2016·American Journal of Epidemiology
DOI 10.1093/aje/kww007
Open this paper in CoChat — free account

Abstract

The placenta plays a crucial role in fetal growth and development through adaptive responses to perturbations of the maternal environment. We investigated the association between placental 3-nitrotyrosine (3-NTp), a biomarker of oxidative stress, and exposure to air pollutants during various time windows of pregnancy. We measured the placental 3-NTp levels of 330 mother-newborn pairs enrolled in the Environmental Influence on Ageing in Early Life (ENVIRONAGE) Study, a Belgian birth cohort study (2010-2013). Daily concentrations of particulate matter with an aerodynamic diameter ≤2.5 µm (PM2.5), black carbon (BC), and nitrogen dioxide were interpolated for each mother's residence using a spatiotemporal interpolation method. Placental 3-NTp levels, adjusted for covariates, increased by 35.0% (95% confidence interval (CI): 13.9, 60.0) for each interquartile-range increment in entire-pregnancy PM2.5 exposure. The corresponding estimate for BC exposure was 13.9% (95% CI: -0.21, 29.9). These results were driven by the first (PM2.5: 29.0% (95% CI: 4.9, 58.6); BC: 23.6% (95% CI: 4.4, 46.4)) and second (PM2.5: 39.3% (95% CI: 12.3, 72.7)) gestational exposure windows. This link between placental nitrosative stress and exposure to fine particle air pollution during gestation is in line with experimental evidence on cigarette smoke and diesel exhaust exposure. Further research is needed to elucidate potential health consequences experienced later in life through particle-mediated nitrosative stress incurred during fetal life.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1093/aje/kww007

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 37

  1. Scheers H, Mwalili SM, Faes C, et al. Does air pollution trigger infant mortality in Western Europe? A case-crossover study. Environ Health Perspect. 2011;119(7):1017-1022.
  2. Pedersen M, Giorgis-Allemand L, Bernard C, et al. Ambient air pollution and low birthweight: a European cohort study (ESCAPE). Lancet Respir Med. 2013;1(9):695-704.
  3. Lakshmanan A, Chiu YH, Coull BA, et al. Associations between prenatal traffic-related air pollution exposure and birth weight: modification by sex and maternal pre-pregnancy body mass index. Environ Res. 2015;137:268-277.
  4. Ballester F, Estarlich M, Iñiguez C, et al. Air pollution exposure during pregnancy and reduced birth size: a prospective birth cohort study in Valencia, Spain. Environ Health. 2010;9:6.
  5. Nawrot TS, Nemmar A, Nemery B. Air pollution: to the heart of the matter. Eur Heart J. 2006;27(19):2269-2271.
  6. Brunekreef B, Holgate ST. Air pollution and health. Lancet. 2002;360(9341):1233-1242.
  7. Rossner P Jr, Svecova V, Milcova A, et al. Oxidative and nitrosative stress markers in bus drivers. Mutat Res. 2007; 617(1-2):23-32.
  8. Lodovici M, Bigagli E. Oxidative stress and air pollution exposure. J Toxicol. 2011;2011:487074.
  9. Risom L, Møller P, Loft S. Oxidative stress-induced DNA damage by particulate air pollution. Mutat Res. 2005;592(1-2): 119-137.
  10. Miller MR, Shaw CA, Langrish JP. From particles to patients: oxidative stress and the cardiovascular effects of air pollution. Future Cardiol. 2012;8(4):577-602.
  11. Ischiropoulos H. Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch Biochem Biophys. 1998;356(1):1-11.
  12. Webster RP, Roberts VH, Myatt L. Protein nitration in placenta- functional significance. Placenta. 2008;29(12):985-994.
  13. Murata M, Kawanishi S. Oxidative DNA damage induced by nitrotyrosine, a biomarker of inflammation. Biochem Biophys Res Commun. 2004;316(1):123-128.
  14. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007;87(1): 315-424.
  15. Souza JM, Choi I, Chen QP, et al. Proteolytic degradation of tyrosine nitrated proteins. Arch Biochem Biophys. 2000;380(2): 360-366.
  16. Grune T, Reinheckel T, Davies KJ. Degradation of oxidized proteins in mammalian cells. FASEB J. 1997;11(7):526-534.
  17. Castegna A, Thongboonkerd V, Klein JB, et al. Proteomic identification of nitrated proteins in Alzheimer's disease brain. J Neurochem. 2003;85(6):1394-1401.
  18. Good PF, Hsu A, Werner P, et al. Protein nitration in Parkinson's disease. J Neuropathol Exp Neurol. 1998;57(4):338-342.
  19. Lyall F, Gibson JL, Greer IA, et al. Increased nitrotyrosine in the diabetic placenta: evidence for oxidative stress. Diabetes Care. 1998;21(10):1753-1758.
  20. Bosco C, González J, Gutiérrez R, et al. Oxidative damage to pre-eclamptic placenta: immunohistochemical expression of VEGF, nitrotyrosine residues and von Willebrand factor. J Matern Fetal Neonatal Med. 2012;25(11):2339-2345. 448 Saenen et al. Am J Epidemiol. 2016;184(6):442-449
  21. Saenen ND, Plusquin M, Bijnens E, et al. In utero fine particle air pollution and placental expression of genes in the brain-derived neurotrophic factor signaling pathway: an ENVIRONAGE birth cohort study. Environ Health Perspect. 2015;123(8):834-840.
  22. Cox B, Martens E, Nemery B, et al. Impact of a stepwise introduction of smoke-free legislation on the rate of preterm births: analysis of routinely collected birth data. BMJ. 2013;346:f441.
  23. Janssen S, Dumont G, Fierens F, et al. Spatial interpolation of air pollution measurements using CORINE land cover data. Atmos Environ. 2008;42(20):4884-4903.
  24. Lefebvre W, Degrawe B, Beckx C, et al. Presentation and evaluation of an integrated model chain to respond to traffic- and health-related policy questions. Environ Model Softw. 2013;40:160-170.
  25. Lefebvre W, Vercauteren J, Schrooten L, et al. Validation of the MIMOSA-AURORA-IFDM model chain for policy support: modeling concentrations of elemental carbon in Flanders. Atmos Environ. 2011;45(37):6705-6713.
  26. Wick P, Malek A, Manser P, et al. Barrier capacity of human placenta for nanosized materials. Environ Health Perspect. 2010;118(3):432-436.
  27. Sandovici I, Hoelle K, Angiolini E, et al. Placental adaptations to the maternal-fetal environment: implications for fetal growth and developmental programming. Reprod Biomed Online. 2012;25(1):68-89.
  28. Veras MM, Damaceno-Rodrigues NR, Caldini EG, et al. Particulate urban air pollution affects the functional morphology of mouse placenta. Biol Reprod. 2008;79(3): 578-584.
  29. Xiao GG, Nel AE, Loo JA. Nitrotyrosine-modified proteins and oxidative stress induced by diesel exhaust particles. Electrophoresis. 2005;26(1):280-292.
  30. Myatt L. Placental adaptive responses and fetal programming. J Physiol. 2006;572(1):25-30.
  31. Weldy CS, Liu Y, Liggitt HD, et al. In utero exposure to diesel exhaust air pollution promotes adverse intrauterine conditions, resulting in weight gain, altered blood pressure, and increased susceptibility to heart failure in adult mice. PLoS One. 2014; 9(2):e88582.
  32. Kunitomo M, Yamaguchi Y, Kagota S, et al. Biochemical evidence of atherosclerosis progression mediated by increased oxidative stress in apolipoprotein E-deficient spontaneously hyperlipidemic mice exposed to chronic cigarette smoke. J Pharmacol Sci. 2009;110(3):354-361.
  33. Mills NL, Robinson SD, Fokkens PH, et al. Exposure to concentrated ambient particles does not affect vascular function in patients with coronary heart disease. Environ Health Perspect. 2008;116(6):709-715.
  34. Clemente DB, Casas M, Vilahur N, et al. Prenatal ambient air pollution, placental mitochondrial DNA content, and birth weight in the INMA (Spain) and ENVIRONAGE (Belgium) birth cohorts. Environ Health Perspect. 2016;124(5):659-665.
  35. Chang HH, Warren JL, Darrow LA, et al. Assessment of critical exposure and outcome windows in time-to-event analysis with application to air pollution and preterm birth study. Biostatistics. 2015;16(3):509-521.
  36. Rappazzo KM, Daniels JL, Messer LC, et al. Exposure to fine particulate matter during pregnancy and risk of preterm birth among women in New Jersey, Ohio, and Pennsylvania, 2000- 2005. Environ Health Perspect. 2014;122(9):992-997.
  37. Robledo CA, Mendola P, Yeung E, et al. Preconception and early pregnancy air pollution exposures and risk of gestational diabetes mellitus. Environ Res. 2015;137:316-322. Placental Nitrosative Stress and Ambient Air Pollution 449 Am J Epidemiol. 2016;184(6):442-449

Cited by

Sorted by citations

Authors
Saenen, N. D., Vrijens, K., Janssen, B. G., Madhloum, N., Peusens, M., Gyselaers, W., Vanpoucke, C., Lefebvre, W., Roels, H. A., & Nawrot, T. S.
Affiliations
Hasselt University (BE)
Corresponding author
Nawrot, Tim S.
ORCID
Venue
American Journal of Epidemiology
Publisher
Oxford University Press (OUP)
Published
2016-09-05
Volume
184
Issue
6
Pages
442-449
ISSN
  • 0002-9262 (ISSN-L)
  • 1476-6256
DOI
10.1093/aje/kww007
OpenAlex
W2510576856
Cited by
112
References
3
Citations by year
2026: 10 · 2025: 15 · 2024: 8 · 2023: 13 · 2022: 12 · 2021: 13 · 2020: 11 · 2019: 11 · 2018: 9 · 2017: 8 · 2016: 2
FWCI
6.28
Type
journal article
Language
en
Open access
closed
Locations
  • American Journal of Epidemiology (publishedVersion)
  • PubMed (publishedVersion)
  • Document Server@UHasselt (UHasselt) (submittedVersion)
  • Lirias (submittedVersion)
  • HighWire Press Open Archive (submittedVersion)
Funders
  • European Research Council (ERC-2012-StG 310898)
  • Flemish Scientific Fund (G.073315N, 12D7714N)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Health, Environment, Cognitive Aging
  • Social Sciences › Sociology and Political Science › Environmental Justice and Health Disparities
Keywords
nitrotyrosine, prenatal air pollution exposure, PM2.5, black carbon, nitrogen dioxide, oxidative stress biomarkers, fetal development, ENVIRONAGE birth cohort
MeSH terms
Adult, Belgium, Female, Humans, Infant, Newborn, Male, Maternal Age, Placenta, Pregnancy, Prenatal Exposure Delayed Effects, Pyrimidines, Smoking, Social Class, Stress, Physiological, Body Mass Index, Maternal Exposure, Particulate Matter

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