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      Maternal exposure to diluted diesel engine exhaust alters placental function and induces intergenerational effects in rabbits

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          Abstract

          Background

          Airborne pollution is a rising concern in urban areas. Epidemiological studies in humans and animal experiments using rodent models indicate that gestational exposure to airborne pollution, in particular diesel engine exhaust (DE), reduces birth weight, but effects depend on exposure duration, gestational window and nanoparticle (NP) concentration. Our aim was to evaluate the effects of gestational exposure to diluted DE on feto-placental development in a rabbit model.

          Pregnant females were exposed to diluted (1 mg/m 3), filtered DE (NP diameter ≈ 69 nm) or clean air (controls) for 2 h/day, 5 days/week by nose-only exposure (total exposure: 20 days in a 31-day gestation).

          Results

          DE exposure induced early signs of growth retardation at mid gestation with decreased head length ( p = 0.04) and umbilical pulse ( p = 0.018). Near term, fetal head length ( p = 0.029) and plasma insulin and IGF1 concentrations ( p = 0.05 and p = 0.019) were reduced. Placental function was also affected, with reduced placental efficiency (fetal/placental weight) ( p = 0.049), decreased placental blood flow ( p = 0.009) and fetal vessel volume ( p = 0.002). Non-aggregated and “fingerprint” NP were observed at various locations, in maternal blood space, in trophoblastic cells and in the fetal blood, demonstrating transplacental transfer. Adult female offspring were bred with control males. Although fetoplacental biometry was not affected near term, second generation fetal metabolism was modified by grand-dam exposure with decreased plasma cholesterol ( p = 0.008) and increased triglyceride concentrations ( p = 0.015).

          Conclusions

          Repeated daily gestational exposure to DE at levels close to urban pollution can affect feto-placental development in the first and second generation.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12989-016-0151-7) contains supplementary material, which is available to authorized users.

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          Most cited references 50

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          Silica and titanium dioxide nanoparticles cause pregnancy complications in mice.

          The increasing use of nanomaterials has raised concerns about their potential risks to human health. Recent studies have shown that nanoparticles can cross the placenta barrier in pregnant mice and cause neurotoxicity in their offspring, but a more detailed understanding of the effects of nanoparticles on pregnant animals remains elusive. Here, we show that silica and titanium dioxide nanoparticles with diameters of 70 nm and 35 nm, respectively, can cause pregnancy complications when injected intravenously into pregnant mice. The silica and titanium dioxide nanoparticles were found in the placenta, fetal liver and fetal brain. Mice treated with these nanoparticles had smaller uteri and smaller fetuses than untreated controls. Fullerene molecules and larger (300 and 1,000 nm) silica particles did not induce these complications. These detrimental effects are linked to structural and functional abnormalities in the placenta on the maternal side, and are abolished when the surfaces of the silica nanoparticles are modified with carboxyl and amine groups.
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            Ambient air pollution and low birthweight: a European cohort study (ESCAPE).

            Ambient air pollution has been associated with restricted fetal growth, which is linked with adverse respiratory health in childhood. We assessed the effect of maternal exposure to low concentrations of ambient air pollution on birthweight. We pooled data from 14 population-based mother-child cohort studies in 12 European countries. Overall, the study population included 74 178 women who had singleton deliveries between Feb 11, 1994, and June 2, 2011, and for whom information about infant birthweight, gestational age, and sex was available. The primary outcome of interest was low birthweight at term (weight <2500 g at birth after 37 weeks of gestation). Mean concentrations of particulate matter with an aerodynamic diameter of less than 2·5 μm (PM2·5), less than 10 μm (PM10), and between 2·5 μm and 10 μm during pregnancy were estimated at maternal home addresses with temporally adjusted land-use regression models, as was PM2·5 absorbance and concentrations of nitrogen dioxide (NO2) and nitrogen oxides. We also investigated traffic density on the nearest road and total traffic load. We calculated pooled effect estimates with random-effects models. A 5 μg/m(3) increase in concentration of PM2·5 during pregnancy was associated with an increased risk of low birthweight at term (adjusted odds ratio [OR] 1·18, 95% CI 1·06-1·33). An increased risk was also recorded for pregnancy concentrations lower than the present European Union annual PM2·5 limit of 25 μg/m(3) (OR for 5 μg/m(3) increase in participants exposed to concentrations of less than 20 μg/m(3) 1·41, 95% CI 1·20-1·65). PM10 (OR for 10 μg/m(3) increase 1·16, 95% CI 1·00-1·35), NO2 (OR for 10 μg/m(3) increase 1·09, 1·00-1·19), and traffic density on nearest street (OR for increase of 5000 vehicles per day 1·06, 1·01-1·11) were also associated with increased risk of low birthweight at term. The population attributable risk estimated for a reduction in PM2·5 concentration to 10 μg/m(3) during pregnancy corresponded to a decrease of 22% (95% CI 8-33%) in cases of low birthweight at term. Exposure to ambient air pollutants and traffic during pregnancy is associated with restricted fetal growth. A substantial proportion of cases of low birthweight at term could be prevented in Europe if urban air pollution was reduced. The European Union. Copyright © 2013 Elsevier Ltd. All rights reserved.
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              Maternal Exposure to Particulate Air Pollution and Term Birth Weight: A Multi-Country Evaluation of Effect and Heterogeneity

              Background: A growing body of evidence has associated maternal exposure to air pollution with adverse effects on fetal growth; however, the existing literature is inconsistent. Objectives: We aimed to quantify the association between maternal exposure to particulate air pollution and term birth weight and low birth weight (LBW) across 14 centers from 9 countries, and to explore the influence of site characteristics and exposure assessment methods on between-center heterogeneity in this association. Methods: Using a common analytical protocol, International Collaboration on Air Pollution and Pregnancy Outcomes (ICAPPO) centers generated effect estimates for term LBW and continuous birth weight associated with PM10 and PM2.5 (particulate matter ≤ 10 and 2.5 µm). We used meta-analysis to combine the estimates of effect across centers (~ 3 million births) and used meta-regression to evaluate the influence of center characteristics and exposure assessment methods on between-center heterogeneity in reported effect estimates. Results: In random-effects meta-analyses, term LBW was positively associated with a 10-μg/m3 increase in PM10 [odds ratio (OR) = 1.03; 95% CI: 1.01, 1.05] and PM2.5 (OR = 1.10; 95% CI: 1.03, 1.18) exposure during the entire pregnancy, adjusted for maternal socioeconomic status. A 10-μg/m3 increase in PM10 exposure was also negatively associated with term birth weight as a continuous outcome in the fully adjusted random-effects meta-analyses (–8.9 g; 95% CI: –13.2, –4.6 g). Meta-regressions revealed that centers with higher median PM2.5 levels and PM2.5:PM10 ratios, and centers that used a temporal exposure assessment (compared with spatiotemporal), tended to report stronger associations. Conclusion: Maternal exposure to particulate pollution was associated with LBW at term across study populations. We detected three site characteristics and aspects of exposure assessment methodology that appeared to contribute to the variation in associations reported by centers.
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                Author and article information

                Contributors
                sarah.valentino@jouy.inra.fr
                anne.tarrade@jouy.inra.fr
                josiane.aioun@jouy.inra.fr
                eve.mourier@jouy.inra.fr
                christophe.richard@jouy.inra.fr
                michele.dahirel@jouy.inra.fr
                delphine.rousseau@jouy.inra.fr
                natalie_fournier@yahoo.fr
                marie-christine.aubriere@jouy.inra.fr
                mslallemand@jouy.inra.fr
                sylvaine.camous@jouy.inra.fr
                marine.guinot@jouy.inra.fr
                madia.charlier@jouy.inra.fr
                etienne.aujean@jouy.inra.fr
                aladhami@unistra.fr
                paul.fokkens@rivm.nl
                lydiane.agier@ujf-grenoble.fr
                john.boere@rivm.nl
                flemming.cassee@rivm.nl
                remy.slama@uij-grenoble.fr
                pascale.chavatte@jouy.inra.fr
                Journal
                Part Fibre Toxicol
                Part Fibre Toxicol
                Particle and Fibre Toxicology
                BioMed Central (London )
                1743-8977
                26 July 2016
                26 July 2016
                2015
                : 13
                Affiliations
                [1 ]UMR BDR, INRA, ENVA, Université Paris Saclay, 78350 Jouy en Josas, France
                [2 ]PremUp Foundation, Paris, France
                [3 ]UFR de Pharmacie, Univ Paris-Sud, EA 4041/4529 Lip (Sys), Châtenay-Malabry, France
                [4 ]Hôpital Européen Georges Pompidou (AP-HP), Laboratoire de Biochimie, UF Cardio-Vasculaire, Paris, France
                [5 ]INRA, UMR1313 Génétique Animale et Biologie Intégrative, Jouy en Josas, France
                [6 ]Centre for Sustainability, Environment and Health, National Institute for Public Health and the Environment, Bilthoven, Netherlands
                [7 ]Inserm and Univ. Grenoble Alpes, U823, IAB Research Center, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, France
                [8 ]Institute of Risk Assessment Sciences, Utrecht University, Utrecht, Netherlands
                Article
                151
                10.1186/s12989-016-0151-7
                4962477
                27460165
                © The Author(s). 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-13-CESA-0011-EPAPP
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: 311765-E-DOHaD
                Award Recipient :
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                Research
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                © The Author(s) 2016

                Toxicology

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