Abstract
Purpose
Polycyclic aromatic hydrocarbons (PAHs) are known for their carcinogenic and teratogenic properties. However, little is known about the effect of PAH on our immune and respiratory systems. Hence, we investigated associations (1) between PAH exposure and IgE levels and asthma in children and (2) between PAH exposure and the oxidative stress marker 8OHdG potentially involved in disease pathogenesis stratifying by (3) sex-based differences.
Methods
A total of 453 kindergarten children were recruited and provided samples. Urine biomarker of PAH exposure (1-OHP levels) was measured by UPLC-MS/MS and a marker of oxidative stress (8OHdG) was measured by ELISA. Serum IgE were assessed and information on asthma was collected. Associations between 1-OHP levels, 8OHdG, IgE and asthma were analyzed by multivariate linear and logistic regression. A mediation analysis was conducted to evaluate whether the risk of increased IgE and asthma related to PAH exposure is explained by 8OHdG changes.
Results
Urine 1-OHP levels were positively related to 8OHdG levels (per ln-unit: β = 0.30kU/l, p = 0.002). Similar results were also found for 1-OHP levels with IgE levels (per ln-unit: β = 0.27 kU/l, p = 0.027). 1-OHP levels (per ln-unit) were significantly associated with asthma, with an OR (95% CI) of 1.42 (1.18–1.70). In addition, 1-OHP levels were associated with asthma. It is estimated that 35% of the effect of PAH exposure on asthma is mediated by 8OHdG levels.
Conclusion
Exposure to PAH may enhance oxidative stress and may induce asthma. The effect of PAH exposure on asthma may be mediated by oxidative stress.
Similar content being viewed by others
References
Al-Daghri NM, Alokail MS, Abd-Alrahman SH, Draz HM, Yakout SM, Clerici M (2013) Polycyclic aromatic hydrocarbon exposure and pediatric asthma in children: a case–control study. Environ Health 12:1
Bae S, Pan XC, Kim SY, Park K, Kim YH, Kim H, Hong YC (2010) Exposures to particulate matter and polycyclic aromatic hydrocarbons and oxidative stress in schoolchildren. Environ Health Perspect 118:579–583
Bagryantseva Y, Novotna B, Rossner P Jr, Chvatalova I, Milcova A, Svecova V, Lnenickova Z, Solansky I, Sram RJ (2010) Oxidative damage to biological macromolecules in Prague bus drivers and garagemen: impact of air pollution andgenetic polymorphisms. Toxicol Lett 199:60–68
Bouchard M, Thuot R, Carrier G, Viau C (2002) Urinary excretion kinetics of 1-hydroxypyrene in rats subchronically exposed to pyrene or polycyclic aromatic hydrocarbon mixtures. J Toxicol Environ Health A 65:1195–1209
Cayman Chemical Company (2012) Creatinine (urinary) assay kit. https://www.caymanchem.com/pdfs/500701.pdf. Accessed 26 July 2016
Cho YS, Moon HB (2010) The role of oxidative stress in the pathogenesis of asthma. Allergy Asthma Immunol Res 2:183–187
de Marco R, Locatelli F, Sunyer J, Burney P (2000) Differences in incidence of reported asthma related to age in men and women. A retrospective analysis of the data of the European Respiratory Health Survey. Am J Respir Crit Care Med 162:68–74
Esposito S, Tenconi R, Lelii M, Preti V, Nazzari E, Consolo S, Patria MF (2014) Possible molecular mechanisms linking air pollution and asthma in children. BMC Pulm Med 14:31
Falcó G, Domingo JL, Llobet JM, Teixidó A, Casas C, Müller L (2003) Polycyclic aromatic hydrocarbons in foods: human exposure through the diet in Catalonia. Spain J Food Prot 66:2325–2331
Fan R, Dong Y, Zhang W, Wang Y, Yu Z, Sheng G, Fu J (2006) Fast simultaneous determination of urinary 1-hydroxypyrene and 3-hydroxybenzo[a]pyrene by liquid chromatography-tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2836:92–97
Han IK (2008) Urinary 1-hydroxypyrene in Nonsmokers: a biomarker for coke smoke exposure and general urban PAH exposure. https://www.researchgate.net/publication/277041287_Urinary_1-hydroxypyrene_in_nonsmokers_a_biomarker_for_coke_smoke_exposure_and_general_urban_PAH_exposure. Accessed 8 Aug 2016
Health Canada (2013) Second Report on Human Biomonitoring of Environmental Chemicals in Canada: Results of the Canadian Health Measures Survey Cycle 2 (2009–2011). Minister of Health, Ottawa. http://www.hc-sc.gc.ca/ewh-semt/pubs/contaminants/chms-ecms/index-eng.php. Accessed 11 Aug 2016
Heudorf U, Angerer J (2001) Internal exposure to PAHs of children and adults living in homes with parquet flooring containing high levels of PAHs in the parquet glue. Int Arch Occup Environ Health 74:91–101
Jedrychowski W, Galas A, Pac A, Flak E, Camman D, Rauh V, Perera F (2005) Prenatal ambient air exposure to polycyclic aromatic hydrocarbons andthe occurrence of respiratory symptoms over the first year of life. Eur J Epidemiol 20:775–782
Jedrychowski WA, Perera FP, Maugeri U, Mrozek-Budzyn D, Mroz E, Klimaszewska-Rembiasz M, Flak E, Edwards S, Spengler J, Jacek R, Sowa A (2010) Intrauterine exposure to polycyclic aromatic hydrocarbons, fine particulate matter and early wheeze: prospective birth cohort study in 4 yearolds. Pediatr Allergy Immunol 21:e723–e732
Jongeneelen FJ (2001) Benchmark guideline for urinary 1-hydroxypyrene as biomarker of occupational exposure to polycyclic aromatic hydrocarbons. Ann Occup Hyg 45:3–13
Jongeneelen FJ, van Leeuwen FE, Oosterink S, Anzion RB, van der Loop F, Bos RP, van Veen HG (1990) Ambient and biological monitoring of coke oven workers: determinants of the internal dose of polycyclic aromatic hydrocarbons. Br J Ind Med 47:454–461
Jung KH, Yan B, Moors K, Chillrud SN, Perzanowski MS, Whyatt RM, Hoepner L, Goldstein I, Zhang B, Camann D, Kinney PL, Perera FP, Miller RL (2012) Repeated exposure to polycyclic aromatic hydrocarbons and asthma: effect of seroatopy. Ann Allergy Asthma Immunol 109:249–254
Karimi P, Peters KO, Bidad K, Strickland PT (2015) Polycyclic aromatic hydrocarbons and childhood asthma. Eur J Epidemiol 30:91–101
Kim JH, Kim JK, Son BK, Oh JE, Lim DH, Lee KH, Hong YC, Cho SI (2005) Effects of air pollutants on childhood asthma. Yonsei Med J 46:239–244
Kim KH, Jahan SA, Kabir E, Brown RJ (2013) A review of airborne polycyclic aromatic hydrocarbons (PAHs) and their human health effects. Environ Int 60:71–80
Leem JH, Kim JH, Lee KH, Hong Yc, Lee KH, Kang D, Kwon HJ (2005) Asthma attack associated with oxidative stress by exposure to ETS and PAH. J Asthma 42:463–467
Li Z, Sandau CD, Romanoff LC, Caudill SP, Sjodin A, Needham LL, Patterson DG Jr (2008) Concentration and profile of 22 urinary polycyclic aromatic hydrocarbon metabolites in the US population. Environ Res 107:320–331
Li N, Wang M, Bramble LA, Schmitz DA, Schauer JJ, Sioutas C, Harkema JR, Nel AE (2009) The adjuvant effect of ambient particulate matter is closely reflected by the particulate oxidant potential. Environ Health Perspect 117:1116–1123.
Lummus ZL, Wisnewski AV, Bernstein DI (2011) Pathogenesis and disease mechanisms of occupational asthma. Immunol Allergy Clin North Am 31:699–716
Miller RL, Garfinkel R, Lendor C, Hoepner L, Li Z, Romanoff L, Sjodin A, Needham L, Perera FP, Whyatt RM (2010) Polycyclic aromatic hydrocarbon metabolite levels and pediatric allergy and asthma in an inner-city cohort. Pediatr Allergy Immunol 21:260–267
Nadeau K, McDonald-Hyman C, Noth EM, Pratt B, Hammond SK, Balmes J, Tager I (2010) Ambient air pollution impairs regulatory T-cell function in asthma. J Allergy Clin Immunol 126:845–852
Perzanowski MS, Chew GL, Divjan A, Jung KH, Ridder R, Tang D, Diaz D, Goldstein IF, Kinney PL, Rundle AG, Camann DE, Perera FP, Miller RL (2013) Early-life cockroach allergen and polycyclic aromatic hydrocarbon exposures predict cockroach sensitization among inner-city children. J Allergy Clin Immunol 131:886–893
Pilger A, Rüdiger HW (2006) 8-Hydroxy-2′-deoxyguanosine as a marker of oxidative DNA damage related to occupational and environmental exposures. Int Arch Occup Environ Health 80:1–15
Preacher KJ, Kelley K (2011) Effect size measures for mediation models: quantitative strategies for communicating indirect effects. Psychol Methods 16:93–115
Rezaee AR, Azadi A, Houshmand M, Mahmoodi F, Purpak Z, Safaei S, Karimi P, Ghabaee M, Sahraian MA (2013) Mitochondrial and nuclear genes as the cause of complex I deficiency. Genet Mol Res 12:3551–3554
Rosa MJ, Jung KH, Perzanowski MS, Kelvin EA, Darling KW, Camann DE, Chillrud SN, Whyatt RM, Kinney PL, Perera FP, Miller RL (2011) Prenatal exposure to polycyclic aromatic hydrocarbons, environmental tobacco smoke and asthma. Respir Med 105:869–876
Seagrave J, Campen MJ, McDonald JD, Mauderly JL, Rohr AC (2008) Oxidative stress, inflammation, and pulmonary function assessment in rats exposed to laboratory-generated pollutant mixtures. J Toxicol Environ Health A 71:1352–1562
Soto-Martínez ME, Avila L, Soto-Quirós ME (2009) New criteria for the diagnosis and management of asthma in children under 5 years old: GINA Guidelines An. An Pediatr (Barc) 71:91–94
Soto-Ramírez N, Ziyab AH, Karmaus W, Zhang H, Kurukulaaratchy RJ, Ewart S, Arshad SH (2013) Epidemiologic methods of assessing asthma and wheezing episodes in longitudinal studies: measures of change and stability. J Epidemiol 23:399–410
Suwan-Ampai P, Navas-Acien A, Strickland PT, Agnew J (2009) Involuntary tobacco smoke exposure and urinary levels of polycyclic aromatic hydrocarbons in the United States, 1999 to 2002. Cancer Epidemiol Biomarkers Prev 18:884–893
Tang D, Li TY, Liu JJ, Chen YH, Qu L, Perera F (2006) PAH-DNA adducts in cord blood and fetal and child development in a Chinese cohort. Environ Health Perspect 114:1297–1300
US EPA (2011) Benzo(a)pyrene. http://www.epa.gov/pbt/pubs/benzo.htm. Accessed 26 Aug 2016
Wang IJ, Lin TJ (2015) FLG P478S polymorphisms and environmental risk factors for the atopic march in Taiwanese children: a prospective cohort study. Ann Allergy Asthma Immunol 114:52–57
Weidinger S, Illig T, Baurecht H, Irvine AD, Rodriguez E, Diaz-Lacava A, Klopp N, Wagenpfeil S, Zhao Y, Liao H, Lee SP, Palmer CN, Jenneck C, Maintz L, Hagemann T, Behrendt H, Ring J, Nothen MM, McLean WH, Novak N (2006) Loss-of-function variations within the filaggrin gene predispose for atopic dermatitis with allergic sensitizations. J Allergy Clin Immunol 118:214–219
Acknowledgements
This study was supported by grants from the Ministry of Health and Welfare and from the Ministry of Science and Technology (MOST 105-2314-B-192-001) in Taiwan. The authors thank the CEAS study group for the data collection.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, IJ., Karmaus, W.J.J. & Yang, CC. Polycyclic aromatic hydrocarbons exposure, oxidative stress, and asthma in children. Int Arch Occup Environ Health 90, 297–303 (2017). https://doi.org/10.1007/s00420-017-1198-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00420-017-1198-y