Occupational exposure and markers of genetic damage, systemic inflammation and lung function: a Danish cross-sectional study among air force personnel

Maria Helena Guerra Andersen, Anne Thoustrup Saber, Marie Frederiksen, Per Axel Clausen, Camilla Sandal Sejbaek, Caroline Hallas Hemmingsen, Niels E Ebbehøj, Julia Catalán, Kukka Aimonen, Joonas Koivisto, Steffen Loft, Peter Møller, Ulla Vogel, Maria Helena Guerra Andersen, Anne Thoustrup Saber, Marie Frederiksen, Per Axel Clausen, Camilla Sandal Sejbaek, Caroline Hallas Hemmingsen, Niels E Ebbehøj, Julia Catalán, Kukka Aimonen, Joonas Koivisto, Steffen Loft, Peter Møller, Ulla Vogel

Abstract

Air force ground crew personnel are potentially exposed to fuels and lubricants, as raw materials, vapours and combustion exhaust emissions, during operation and maintenance of aircrafts. This study investigated exposure levels and biomarkers of effects for employees at a Danish air force military base. We enrolled self-reported healthy and non-smoking employees (n = 79) and grouped them by exposure based on job function, considered to be potentially exposed (aircraft engineers, crew chiefs, fuel operators and munition specialists) or as reference group with minimal occupational exposure (avionics and office workers). We measured exposure levels to polycyclic aromatic hydrocarbons (PAHs) and organophosphate esters (OPEs) by silicone bands and skin wipes (PAHs only) as well as urinary excretion of PAH metabolites (OH-PAHs). Additionally, we assessed exposure levels of ultrafine particles (UFPs) in the breathing zone for specific job functions. As biomarkers of effect, we assessed lung function, plasma levels of acute phase inflammatory markers, and genetic damage levels in peripheral blood cells. Exposure levels of total PAHs, OPEs and OH-PAHs did not differ between exposure groups or job functions, with low correlations between PAHs in different matrices. Among the measured job functions, the UFP levels were higher for the crew chiefs. The exposure level of the PAH fluorene was significantly higher for the exposed group than the reference group (15.9 ± 23.7 ng/g per 24 h vs 5.28 ± 7.87 ng/g per 24 h, p = 0.007), as was the OPE triphenyl phosphate (305 ± 606 vs 19.7 ± 33.8 ng/g per 24 h, p = 0.011). The OPE tris(1,3-dichlor-2-propyl)phosphate had a higher mean in the exposed group (60.7 ± 135 ng/g per 24 h) compared to the reference group (8.89 ± 15.7 ng/g per 24 h) but did not reach significance. No evidence of effects for biomarkers of systemic inflammation, genetic damage or lung function was found. Overall, our biomonitoring study show limited evidence of occupational exposure of air force ground crew personnel to UFPs, PAHs and OPEs. Furthermore, the OH-PAHs and the assessed biomarkers of early biological effects did not differ between exposed and reference groups.

Conflict of interest statement

The authors declare no competing interests.

© 2021. The Author(s).

Figures

Figure 1
Figure 1
Exposure markers levels by job function: (a) PAHs in silicone bands (n = 77); (b) PAHs in skin wipes (n = 54), (c) OPEs in silicone bands (n = 77) and (d) OH-PAHs in urine (n = 78); Dots represent individual measurements and boxplot represent median and interquartile range (25–75%). PAHs, polycyclic aromatic hydrocarbons; OPEs, organophosphate esters; OH-PAHs, monohydroxylated metabolites of PAHs.
Figure 2
Figure 2
Effect marker levels per job function: (a) DNA strand breaks (n = 77); (b) Frequency of micronucleated + CD71 reticulocytes (n = 70); (c) Inflammation CRP (n = 65); (d) Inflammation SAA (n = 65); (e) Lung function FEV1 (n = 65); (f) Lung function FVC (n = 65). Dots represent individual measurements and boxplots represent interquartile range (25–75%). CRP, C-reactive protein; SAA, serum amyloid A; FEV1, forced expiratory volume in 1 s; FEV, forced vital capacity.

References

    1. National Research Council. In Toxicologic Assessment of Jet-Propulsion Fuel 8 (National Academies Press, 2003).
    1. IARC. Occupational Exposures in Petroleum Refining; Crude Oil and Major Petroleum Fuels. 1–331 (World Health Organization—International Agency for Research on Cancer, 1989).
    1. Ritchie G, et al. Biological and health effects of exposure to kerosene-based jet fuels and performance additives. J. Toxicol. Environ. Health B Crit. Rev. 2003;6:357–451. doi: 10.1080/10937400306473.
    1. Bendtsen, K. M., Bengtsen, E., Saber, A. T. & Vogel, U. A review of health effects associated with exposure to jet engine emissions in and around airports. Environ. Health (in press) (2021).
    1. Li WH, Wang Y, Kannan K. Occurrence, distribution and human exposure to 20 organophosphate esters in air, soil, pine needles, river water, and dust samples collected around an airport in New York state, United States. Environ. Int. 2019 doi: 10.1016/j.envint.2019.105054.
    1. Saillenfait AM, Ndaw S, Robert A, Sabate JP. Recent biomonitoring reports on phosphate ester flame retardants: a short review. Arch. Toxicol. 2018;92:2749–2778. doi: 10.1007/s00204-018-2275-z.
    1. van der Veen I, de Boer J. Phosphorus flame retardants: properties, production, environmental occurrence, toxicity and analysis. Chemosphere. 2012;88:1119–1153. doi: 10.1016/j.chemosphere.2012.03.067.
    1. Bendtsen KM, et al. Airport emission particles: exposure characterization and toxicity following intratracheal instillation in mice. Part Fibre Toxicol. 2019;16:23. doi: 10.1186/s12989-019-0305-5.
    1. Andersen MHG, et al. Association between polycyclic aromatic hydrocarbon exposure and peripheral blood mononuclear cell DNA damage in human volunteers during fire extinction exercises. Mutagenesis. 2018;33:105–115. doi: 10.1093/mutage/gex021.
    1. Andersen MHG, et al. Health effects of exposure to diesel exhaust in diesel-powered trains. Part Fibre Toxicol. 2019;16:21. doi: 10.1186/s12989-019-0306-4.
    1. Hansen AM, Mathiesen L, Pedersen M, Knudsen LE. Urinary 1-hydroxypyrene (1-HP) in environmental and occupational studies—a review. Int. J Hyg. Environ. Health. 2008;211:471–503. doi: 10.1016/j.ijheh.2007.09.012.
    1. Madsen AM, Thilsing T, Baelum J, Garde AH, Vogel U. Occupational exposure levels of bioaerosol components are associated with serum levels of the acute phase protein Serum Amyloid A in greenhouse workers. Environ. Health. 2016;15:9. doi: 10.1186/s12940-016-0090-7.
    1. Jackson P, et al. Validation of freezing tissues and cells for analysis of DNA strand break levels by comet assay. Mutagenesis. 2013;28:699–707. doi: 10.1093/mutage/get049.
    1. Forchhammer L, et al. Variation in the measurement of DNA damage by comet assay measured by the ECVAG inter-laboratory validation trial. Mutagenesis. 2010;25:113–123. doi: 10.1093/mutage/gep048.
    1. Abramsson-Zetterberg L, Zetterberg G, Bergqvist M, Grawe J. Human cytogenetic biomonitoring using flow-cytometric analysis of micronuclei in transferrin-positive immature peripheral blood reticulocytes. Environ. Mol. Mutagen. 2000;36:22–31. doi: 10.1002/1098-2280(2000)36:1<22::AID-EM4>;2-U.
    1. Gerds, T. A. & Ozenne, B. (R package version, 2019).
    1. Moller P, Stopper H, Collins AR. Measurement of DNA damage with the comet assay in high-prevalence diseases: current status and future directions. Mutagenesis. 2020;35:5–18. doi: 10.1093/mutage/gez018.
    1. Moller P, Wallin H, Holst E, Knudsen LE. Sunlight-induced DNA damage in human mononuclear cells. FASEB J. 2002;16:45–53. doi: 10.1096/fj.01-0386com.
    1. Dossing M, Loft S, Schroeder E. Jet fuel and liver function. Scand. J. Work Environ. Health. 1985;11:433–437. doi: 10.5271/sjweh.2203.
    1. Buonanno G, Bernabei M, Avino P, Stabile L. Occupational exposure to airborne particles and other pollutants in an aviation base. Environ. Pollut. 2012;170:78–87. doi: 10.1016/j.envpol.2012.05.027.
    1. Chao YC, et al. Dermal exposure to jet fuel JP-8 significantly contributes to the production of urinary naphthols in fuel-cell maintenance workers. Environ. Health Perspect. 2006;114:182–185. doi: 10.1289/ehp.8288.
    1. Erdem O, Sayal A, Eken A, Akay C, Aydin A. Evaluation of genotoxic and oxidative effects in workers exposed to jet propulsion fuel. Int. Arch. Occup. Environ. Health. 2012;85:353–361. doi: 10.1007/s00420-011-0676-x.
    1. Rodrigues EG, et al. Urinary polycyclic aromatic hydrocarbon (OH-PAH) metabolite concentrations and the effect of GST polymorphisms among US Air Force personnel exposed to jet fuel. J. Occup. Environ. Med. 2014;56:465–471. doi: 10.1097/JOM.0000000000000142.
    1. Serdar B, Egeghy PP, Waidyanatha S, Gibson R, Rappaport SM. Urinary biomarkers of exposure to jet fuel (JP-8) Environ. Health Perspect. 2003;111:1760–1764. doi: 10.1289/ehp.6275.
    1. Smith KW, Proctor SP, Ozonoff AL, McClean MD. Urinary biomarkers of occupational jet fuel exposure among Air Force personnel. J. Expo Sci. Environ. Epidemio.l. 2012;22:35–45. doi: 10.1038/jes.2011.38.
    1. Li Z, et al. Excretion profiles and half-lives of ten urinary polycyclic aromatic hydrocarbon metabolites after dietary exposure. Chem. Res. Toxicol. 2012;25:1452–1461. doi: 10.1021/tx300108e.
    1. Dixon HM, et al. Discovery of common chemical exposures across three continents using silicone wristbands. R. Soc. Open Sci. 2019 doi: 10.1098/rsos.181836.
    1. Hammel SC, Hoffman K, Webster TF, Anderson KA, Stapleton HM. Measuring personal exposure to organophosphate flame retardants using silicone wristbands and hand wipes. Environ. Sci. Technol. 2016;50:4483–4491. doi: 10.1021/acs.est.6b00030.
    1. Hardos, J. E., Rubenstein, M. & Pfahler, S. Organophosphate skin exposure and biological burden of aircraft maintainers. (Air Force Research Laboratory, 711th Human Performance Wing, U.S. Air Force School of Aerospace MedicineOccupational & Environmental Health Dept., Accessed on November 2020.
    1. Hardos JE, Rubenstein M, Pfahler S, Sleight T. Cholinesterase inhibition and exposure to organophosphate esters in aircraft maintenance workers. Aerosp. Med. Hum. Perform. 2020;91:710–714. doi: 10.3357/AMHP.5439.2020.
    1. Khera A, et al. Race and gender differences in C-reactive protein levels. J. Am. Coll. Cardiol. 2005;46:464–469. doi: 10.1016/j.jacc.2005.04.051.
    1. Azqueta A, et al. Application of the comet assay in human biomonitoring: an hCOMET perspective. Mutat. Res. 2020;783:108288. doi: 10.1016/j.mrrev.2019.108288.
    1. LoMauro A, Aliverti A. Sex differences in respiratory function. Breathe (Sheff) 2018;14:131–140. doi: 10.1183/20734735.000318.
    1. Jylhava J, et al. Serum amyloid A is independently associated with metabolic risk factors but not with early atherosclerosis: the Cardiovascular Risk in Young Finns Study. J. Intern. Med. 2009;266:286–295. doi: 10.1111/j.1365-2796.2009.02120.x.
    1. Pitsavos C, Panagiotakos DB, Chrysohoou C, Kavouras S, Stefanadis C. The associations between physical activity, inflammation, and coagulation markers, in people with metabolic syndrome: the ATTICA study. Eur. J. Cardiovac. Prev. Rehabil. 2005;12:151–158. doi: 10.1097/00149831-200504000-00010.
    1. Andersen MHG, et al. Assessment of polycyclic aromatic hydrocarbon exposure, lung function, systemic inflammation, and genotoxicity in peripheral blood mononuclear cells from firefighters before and after a work shift. Environ. Mol. Mutagen. 2018 doi: 10.1002/em.22193.
    1. Lemasters GK, et al. Genotoxic changes after low-level solvent and fuel exposure on aircraft maintenance personnel. Mutagenesis. 1997;12:237–243. doi: 10.1093/mutage/12.4.237.
    1. Pitarque M, Creus A, Marcos R, Hughes JA, Anderson D. Examination of various biomarkers measuring genotoxic endpoints from Barcelona airport personnel. Mutat. Res. 1999;440:195–204. doi: 10.1016/s1383-5718(99)00026-1.
    1. Krieg EF, Jr, et al. Detection of DNA damage in workers exposed to JP-8 jet fuel. Mutat. Res. 2012;747:218–227. doi: 10.1016/j.mrgentox.2012.05.005.
    1. Cavallo D, et al. Occupational exposure in airport personnel: characterization and evaluation of genotoxic and oxidative effects. Toxicology. 2006;223:26–35. doi: 10.1016/j.tox.2006.03.003.
    1. ECHA. Draft screening report: an assessment of wether the use of TCEP, TCPP and TDCP in articles should be restricted. (European Chemicals Agency. . Assessed on November 2020 (2017).
    1. WHO. Flame retardants: Tris(chloropropyl)phosphate and Tris(2-chloroethyl)phosphate. ( Assessed on November 2020 (1998).
    1. Lassen, C. & Lokke, S. Brominated Flame Retardants: Substance Flow Analysis and Assessment of Alternatives. (Danish Environmental Protection Agency, Assessed on November 2020 (1999).
    1. Zhang Y, et al. Impact of mixture effects between emerging organic contaminants on cytotoxicity: a systems biological understanding of synergism between tris(1,3-dichloro-2-propyl)phosphate and triphenyl phosphate. Environ. Sci. Technol. 2020;54:10722–10734. doi: 10.1021/acs.est.0c02188.
    1. Sweeney LM, Prues SL, Reboulet JE. Subacute effects of inhaled Jet Fuel-A (Jet A) on airway and immune function in female rats. Inhal. Toxicol. 2013;25:257–271. doi: 10.3109/08958378.2013.780191.
    1. Canbaz D, Logiantara A, van Ree R, van Rijt LS. Immunotoxicity of organophosphate flame retardants TPHP and TDCIPP on murine dendritic cells in vitro. Chemosphere. 2017;177:56–64. doi: 10.1016/j.chemosphere.2017.02.149.

Source: PubMed

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