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Mitochondrial oxidative DNA damage and exposure to particulate air pollution in mother-newborn pairs
Open accessAbstract
BACKGROUND: Studies emphasize the importance of particulate matter (PM) in the formation of reactive oxygen species and inflammation. We hypothesized that PM exposure during different time windows in pregnancy influences mitochondrial 8-hydroxy-2'-deoxyguanosine (8-OHdG) levels, which is an established biomarker for oxidative stress, in both maternal and foetal blood. METHODS: We investigated maternal (n = 224) and cord blood (n = 293) from mother-newborn pairs that were enrolled in the ENVIRONAGE birth cohort. We determined mitochondrial 8-OHdG by quantitative polymerase chain reaction (qPCR). Multivariable regression models were used to assess the association between mitochondrial 8-OHdG with PM10 and PM2.5 exposure over various time windows during pregnancy. RESULTS: In multivariable analysis, PM10 exposure during the entire pregnancy was positively associated with levels of mitochondrial 8-OHdG in maternal blood. For an IQR increment in PM10 exposure an increase of 18.3 % (95 % confidence interval (CI): 5.6 to 33.4 %, p = 0.004) in 8-OHdG was observed. PM10 exposure during the last trimester of pregnancy was positively associated with levels of 8-OHdG (28.1, 95 % CI: 8.6 to 51.2 %, p = 0.004, for an IQR increment in PM10). In a similar way, PM2.5 exposure was significantly associated with an increase of mitochondrial 8-OHdG levels in maternal blood during the entire pregnancy (13.9, 95 % CI: 0.4 to 29.4 %, p = 0.04 for an IQR increment in PM2.5 exposure) and third trimester of pregnancy (28.1, 95 % CI: 3.6 to 58.4 %, p = 0.02 for an IQR increment in PM2.5 exposure). In umbilical cord blood, 8-OHdG levels were significantly associated with PM10 exposure during first and second trimester of pregnancy with respectively an increase of 23.0 % (95 % CI: 5.9 to 42.8 %, p = 0.007) and 16.6 % (95 % CI: 1.8 to 33.5 %, p = 0.03) for an IQR increment in PM10 exposure. CONCLUSIONS: We found PM-associated increased mitochondrial oxidative DNA damage during pregnancy in both mothers and their newborns. Accordingly, our study showed that particulate air pollution exposure in early life plays a role in increasing systemic oxidative stress, at the level of the mitochondria, both in mother and foetus.
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“Grevendonk et al. [161] demonstrated PM2.5 exposure during pregnancy was positively associated with markers of mitochondrial DNA damage in maternal blood.”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [161]
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Citations
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“Consistent with our results, most of these studies observed a positive association between nuclear 8-OHdG levels in urine and PM exposure [14–16, 23–25] or tobacco smoke exposure [16, 26–29].”
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“Consistent with our results, most of these studies observed a positive association between nuclear 8-OHdG levels in urine and PM exposure [14–16, 23–25] or tobacco smoke exposure [16, 26–29].”
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“If accumulation of 8-OHdG and somatic mtDNA mutations exceed a critical threshold, they can cause a biochemical defect in the mitochondrial respiratory chain and could result in a progressive decline of mitochondrial function [10, 34, 36].”
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“Consistent with our results, most of these studies observed a positive association between nuclear 8-OHdG levels in urine and PM exposure [14–16, 23–25] or tobacco smoke exposure [16, 26–29].”
ResultRoles of oxidative stress in signaling and inflammation induced by particulate matter
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“Pregnancy is a state of increased physiological oxidative stress [5], and maternal exposure to particulate air pollution might exacerbate oxidative damage [1].”
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BackgroundSelf-citationPreconception and early pregnancy air pollution exposures and risk of gestational diabetes mellitus
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“Consistent with our results, most of these studies observed a positive association between nuclear 8-OHdG levels in urine and PM exposure [14–16, 23–25] or tobacco smoke exposure [16, 26–29].”
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“real-time polymerase chain reaction (qPCR) as previously described in detail [11, 21].”
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Self-citationOxidant damage to DNA and pregnancy outcome
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“outcomes such as gestational diabetes mellitus [39] and preeclampsia [40].”
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“risk factor for the induction of inflammatory and oxidative stress responses [1–4], especially during the pregnancy period when increased levels of oxidative stress can be expected [5].”
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“Early and mid-pregnancy exposure windows are critical for adverse newborn health outcomes, including preterm birth [32] and increased risk of gestational diabetes mellitus [33].”
BackgroundOxidative stress and inflammation in pregnancy
Fialová, L., Malbohan, I., Kalousová, M., Soukupová, J., Krofta, L., Štípek, S., & Zima, T. (2006) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365510500375230 · Cited by 76 · cited 2×
“risk factor for the induction of inflammatory and oxidative stress responses [1–4], especially during the pregnancy period when increased levels of oxidative stress can be expected [5].”
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“Several studies demonstrated an association between nuclear 8-OHdG levels and PM exposure [12–16] but whether exposure to PM during gestation influences mitochondrial 8-OHdG both in mothers and newborns is not known.”
BackgroundResultOxidative DNA Damage in Early Pregnancy and Risk of Gestational Diabetes Mellitus: A Pilot Study
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“outcomes such as gestational diabetes mellitus [39] and preeclampsia [40].”
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“If accumulation of 8-OHdG and somatic mtDNA mutations exceed a critical threshold, they can cause a biochemical defect in the mitochondrial respiratory chain and could result in a progressive decline of mitochondrial function [10, 34, 36].”
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“Consistent with our results, most of these studies observed a positive association between nuclear 8-OHdG levels in urine and PM exposure [14–16, 23–25] or tobacco smoke exposure [16, 26–29].”
Result
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Mechanisms of ultrafine particle-induced respiratory health effects
Leikauf, G. D., Kim, S., & Jang, A. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-0394-0 · Cited by 345
Saenen, N. D., Martens, D. S., Neven, K. Y., Alfano, R., Bové, H., Janssen, B. G., Roels, H. A., Plusquin, M., Vrijens, K., & Nawrot, T. S. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0688-z · Cited by 267
Self-citationPrenatal Air Pollution and Newborns' Predisposition to Accelerated Biological Aging
Martens, D. S., Cox, B., Janssen, B. G., Clemente, D. B. P., Gasparrini, A., Vanpoucke, C., Lefebvre, W., Roels, H. A., Plusquin, M., & Nawrot, T. S. (2017) · JAMA Pediatrics · doi:10.1001/jamapediatrics.2017.3024 · Cited by 241
Self-citationImpact of ambient PM2.5 on adverse birth outcome and potential molecular mechanism
Li, Z., Tang, Y., Song, X., Lazar, L., Li, Z., & Zhao, J. (2019) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2018.10.109 · Cited by 193
Metadata
- Authors
- Grevendonk, L., Janssen, B. G., Vanpoucke, C., Lefebvre, W., Hoxha, M., Bollati, V., & Nawrot, T. S.
- Affiliations
- University of Milan (IT)
- Hasselt University (BE)
- Flemish Institute for Technological Research (BE)
- Corresponding author
- Nawrot, Tim S.
- Venue
- Environmental Health
- Published
- 2016-01-20
- Volume
- 15
- Issue
- 1
- Pages
- 10-10
- ISSN
- 1476-069X (ISSN-L)
- PMC
- PMC4719654
- OpenAlex
- W2286090902
- Cited by
- 145
- References
- 43
- Citations by year
- 2026: 6 · 2025: 17 · 2024: 13 · 2023: 16 · 2022: 16 · 2021: 28 · 2020: 8 · 2019: 13 · 2018: 12 · 2017: 12 · 2016: 4
- FWCI
- 8.59
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Environmental Health (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Lirias (KU Leuven) (submittedVersion, cc-by)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Document Server@UHasselt (UHasselt) (submittedVersion, cc-by)
- Funders
- EU Programme “Ideas” (ERC-2011-StG 282413)
- EU Program “Ideas” (ERC-2012-StG 310898)
- Flemish Scientific Fund (FWO) (N1516112/G.0.873.11.N.10)
- 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
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Indoor Air Quality and Microbial Exposure
- Keywords
- particulate matter, PM10, PM2.5, prenatal air pollution exposure, 8-hydroxy-2'-deoxyguanosine, oxidative stress, maternal blood, umbilical cord blood, pregnancy trimesters, ENVIRONAGE birth cohort, prenatal exposure, birth cohort studies, biomarkers of exposure, inflammation, reactive oxygen species
- MeSH terms
- Adult, Air Pollutants, DNA, Mitochondrial, Environmental Exposure, Female, Fetal Blood, Humans, Infant, Newborn, Placenta, Pregnancy, Cohort Studies, Maternal Exposure, Particulate Matter, Young Adult
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