Abstract
Background
Polycyclic aromatic hydrocarbons (PAHs) are environmental pollutants that are potentially hazardous to human health. Dietary exposure is recognized as one of the major pathways of exposure to PAHs among humans. While some PAH exposures have been associated with metabolic syndrome (MetS) in the general population, most epidemiological studies are based on urinary metabolites of a few noncarcinogenic PAHs.
Objective
To investigate the association between estimates of dietary exposure to major carcinogenic PAHs and MetS in Korean adults.
Methods
Multi-cycle Korean National Health and Nutrition Examination Survey (KNHANES) database (n = 16,015) and PAH measurement data from the total diet survey were employed to estimate daily PAH intake for each participating adult. After adjusting for potential confounders, multinomial logistic regression analysis was used to calculate the odds ratios (ORs) and 95% confidence intervals (CIs) between PAHs and MetS of the participating adults.
Results
Benzo(a)pyrene exposure was associated with an increased risk of MetS in men (OR = 1.30; 95% Cl: 1.03–1.63; P-trend = 0.03). In women, however, only chrysene and low high-density lipoprotein (HDL-c) were positively associated with an increased risk of MetS (OR = 1.24; 95% CI: 1.03–1.48; P-trend = 0.0172). Among men, smokers were at an increased risk for MetS, regardless of whether they were exposed to low or high total PAHs and benzo(a)pyrene levels.
Significance
Our findings suggested that PAHs are associated with the risk of MetS and MetS components in Korean adults. In particular, it was confirmed that smoking may influence the relationship between PAH exposure and MetS.Further prospective cohort studies are required to confirm the causal relationship between PAHs and MetS.
Impact statement
Epidemiological studies on PAH exposure are often hampered by a lack of reliable exposure estimates, as biomonitoring of urine does not capture exposure to more toxic PAHs. Using multi-cycle KNHANES data and the measurement data from a total diet survey of Korea, we could develop a personalized PAH intake estimate for each participating adult and assessed the association with MetS.
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Data availability
The data generated in this study were obtained from the Korean National Health and Nutrition Examination Survey (KNHANES), http://knhanes.cdc.go.kr.
References
Abdel-Shafy HI, Mansour MSM. A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet. 2016;25:107–23.
Patel AB, Shaikh S, Jain KR, Desai C, Madamwar D. Polycyclic aromatic hydrocarbons: sources, toxicity, and remediation approaches. Front Microbiol. 2020;11:562813.
Duan X, Shen G, Yang H, Tian J, Wei F, Gong J, et al. Dietary intake polycyclic aromatic hydrocarbons (PAHs) and associated cancer risk in a cohort of Chinese urban adults: Inter- and intra-individual variability. Chemosphere. 2016;144:2469–75.
Rey-Salgueiro L, Martínez-Carballo E, García-Falcón MS, Simal-Gándara J. Effects of a chemical company fire on the occurrence of polycyclic aromatic hydrocarbons in plant foods. Food Chem. 2008;108:347–53.
Srogi K. Monitoring of environmental exposure to polycyclic aromatic hydrocarbons: a review. Environ Chem Lett. 2007;5:169–95.
Zhang B, Pan B, Zhao X, Fu Y, Li X, Yang A, et al. The interaction effects of smoking and polycyclic aromatic hydrocarbons exposure on the prevalence of metabolic syndrome in coke oven workers. Chemosphere. 2020;247:125880.
Huang PL. A comprehensive definition for metabolic syndrome. Dis Model Mech. 2009;2:231–7.
Borch-Johnsen K. The metabolic syndrome in a global perspective. The public health impact–secondary publication. Dan Med Bull. 2007;54:157–9.
O’Neill S, O’Driscoll L. Metabolic syndrome: a closer look at the growing epidemic and its associated pathologies. Obes Rev. 2015;16:1–12.
Bae Y-J. Cereal intake status and nutritional status of adults: results from the Korean National Health and Nutrition Examination Survey, 2013 ~ 2016. J Nutr Health. 2018;51:515–25.
Le Magueresse-Battistoni B, Vidal H, Naville D. Environmental pollutants and metabolic disorders: the multi-exposure scenario of life. Front Endocrinol. 2018;9:582.
Scinicariello F, Buser MC. Urinary polycyclic aromatic hydrocarbons and childhood obesity: NHANES (2001-2006). Environ Health Perspect. 2014;122:299–303.
Wang B, Li Z, Ma Y, Qiu X, Ren A. Association of polycyclic aromatic hydrocarbons in housewives’ hair with hypertension. Chemosphere. 2016;153:315–21.
Jung KH, Perzanowski M, Rundle A, Moors K, Yan B, Chillrud SN, et al. Polycyclic aromatic hydrocarbon exposure, obesity and childhood asthma in an urban cohort. Environ Res. 2014;128:35–41.
Hou J, Sun H, Huang X, Zhou Y, Zhang Y, Yin W, et al. Exposure to polycyclic aromatic hydrocarbons and central obesity enhanced risk for diabetes among individuals with poor lung function. Chemosphere. 2017;185:1136–43.
Lu L, Mackay DF, Pell JP. Meta-analysis of the association between cigarette smoking and peripheral arterial disease. Heart. 2014;100:414–23.
Lu L, Johnman C, McGlynn L, Mackay DF, Shiels PG, Pell JP. Association between exposure to second-hand smoke and telomere length: cross-sectional study of 1303 non-smokers. Int J Epidemiol. 2017;46:1978–84.
Slagter SN, van Vliet-Ostaptchouk JV, Vonk JM, Boezen HM, Dullaart RP, Kobold AC, et al. Associations between smoking, components of metabolic syndrome and lipoprotein particle size. BMC Med. 2013;11:195.
Keith RJ, Al Rifai M, Carruba C, De Jarnett N, McEvoy JW, Bhatnagar A, et al. Tobacco use, insulin resistance, and risk of type 2 diabetes: results from the multi-ethnic study of atherosclerosis. PLoS One. 2016;11:e0157592.
Lee K, Choi K. Non-carcinogenic health outcomes associated with polycyclic aromatic hydrocarbons (PAHs) exposure in humans: an umbrella review. Expos Health. 2023;15:95–111.
Hu H, Kan H, Kearney GD, Xu X. Associations between exposure to polycyclic aromatic hydrocarbons and glucose homeostasis as well as metabolic syndrome in nondiabetic adults. Sci Total Environ. 2015;505:56–64.
Li K, Yin R, Wang Y, Zhao D. Associations between exposure to polycyclic aromatic hydrocarbons and metabolic syndrome in U.S. adolescents: Cross-sectional results from the National Health and Nutrition Examination Survey (2003-2016) data. Environ Res. 2021;202:111747.
Kweon S, Kim Y, Jang MJ, Kim Y, Kim K, Choi S, et al. Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol. 2014;43:69–77.
Amirdivani S, Khorshidian N, Ghobadi Dana M, Mohammadi R, Mortazavian AM, Quiterio de Souza SL, et al. Polycyclic aromatic hydrocarbons in milk and dairy products. Int J Dairy Technol. 2019;72:120–31.
Humans IWGotEoCRt. Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Monogr Eval Carcinog Risks Hum. 2010;92:1–853.
Ishizaki A, Saito K, Hanioka N, Narimatsu S, Kataoka H. Determination of polycyclic aromatic hydrocarbons in food samples by automated on-line in-tube solid-phase microextraction coupled with high-performance liquid chromatography-fluorescence detection. J Chromatogr A. 2010;1217:5555–63.
EFSA, European Food Safety Authority. Polycyclic aromatic hydrocarbons in food: Scientific opinion of the panel on contaminants in the food chain. EFSA J. 2008;724:1–114.
Nguyen KH, Pyo H, Kim J, Shin E, Chang YS. Exposure of general population to PBDEs: a Progressive Total Diet Study in South Korea. Environ Pollut. 2014;195:192–201.
Kim CI, Lee J, Kwon S, Yoon HJ. Total diet study: for a closer-to-real estimate of dietary exposure to chemical substances. Toxicol Res. 2015;31:227–40.
Nisbet IC, LaGoy PK. Toxic equivalency factors (TEFs) for polycyclic aromatic hydrocarbons (PAHs). Regul Toxicol Pharm. 1992;16:290–300.
Kim HS, Kim J, Choi J, Paik Y, Moon B, Joo YS, et al. Polycyclic aromatic hydrocarbons in beverage and dairy products in South Korea: a risk characterization using the total diet study. Food Sci Biotechnol. 2021;30:989–1002.
EU Commission regulation (EU). 2015/1125 of 10 July 2015 amending regulation (EC) No 1881/2006 as regards maximum levels for polycyclic aromatic hydrocarbons in Katsuobushi (dried bonito) and certain smoked Baltic herring. Off J Eur Union. 2015;184:7–10.
Chackrewarthy S, Gunasekera D, Pathmeswaren A, Wijekoon CN, Ranawaka UK, Kato N, et al. A comparison between revised NCEP ATP III and IDF definitions in diagnosing metabolic syndrome in an urban Sri Lankan population: the ragama health study. ISRN Endocrinol. 2013;2013:320176.
Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005;112:2735–52.
Park SY, Freedman ND, Haiman CA, Le Marchand L, Wilkens LR, Setiawan VW. Association of coffee consumption with total and cause-specific mortality among nonwhite populations. Ann Intern Med. 2017;167:228–35.
Kim JH, Yamaguchi K, Lee SH, Tithof PK, Sayler GS, Yoon JH, et al. Evaluation of polycyclic aromatic hydrocarbons in the activation of early growth response-1 and peroxisome proliferator activated receptors. Toxicol Sci. 2005;85:585–93.
Cavalieri E, Rogan E. The molecular etiology and prevention of estrogen-initiated cancers: Ockham’s Razor: Pluralitas non est ponenda sine necessitate. Plurality should not be posited without necessity. Mol Asp Med. 2014;36:1–55.
Kennedy DO, Agrawal M, Shen J, Terry MB, Zhang FF, Senie RT, et al. DNA repair capacity of lymphoblastoid cell lines from sisters discordant for breast cancer. J Natl Cancer Inst. 2005;97:127–32.
Amadou A, Praud D, Coudon T, Deygas F, Grassot L, Faure E, et al. Risk of breast cancer associated with long-term exposure to benzo[a]pyrene (BaP) air pollution: Evidence from the French E3N cohort study. Environ Int. 2021;149:106399.
Biljes D, Hammerschmidt-Kamper C, Kadow S, Diel P, Weigt C, Burkart V, et al. Impaired glucose and lipid metabolism in ageing aryl hydrocarbon receptor deficient mice. EXCLI J. 2015;14:1153–63.
Schulz E, Anter E, Keaney JF Jr. Oxidative stress, antioxidants, and endothelial function. Curr Med Chem. 2004;11:1093–104.
Penning TM. Human aldo-keto reductases and the metabolic activation of polycyclic aromatic hydrocarbons. Chem Res Toxicol. 2014;27:1901–17.
Taddei S, Virdis A, Ghiadoni L, Sudano I, Salvetti A. Endothelial dysfunction in hypertension. J Cardiovasc Pharm. 2001;38:S11–4.
Esser C, Rannug A. The aryl hydrocarbon receptor in barrier organ physiology, immunology, and toxicology. Pharm Rev. 2015;67:259–79.
Brinchmann BC, Le Ferrec E, Podechard N, Lagadic-Gossmann D, Shoji KF, Penna A, et al. Lipophilic chemicals from diesel exhaust particles trigger calcium response in human endothelial cells via aryl hydrocarbon receptor non-genomic signalling. Int J Mol Sci. 2018;19:5.
Bansal S, Leu AN, Gonzalez FJ, Guengerich FP, Chowdhury AR, Anandatheerthavarada HK, et al. Mitochondrial targeting of cytochrome P450 (CYP) 1B1 and its role in polycyclic aromatic hydrocarbon-induced mitochondrial dysfunction. J Biol Chem. 2014;289:9936–51.
Xu X, Li R, Chen G, Hoopes SL, Zeldin DC, Wang DW. The role of cytochrome P450 epoxygenases, soluble epoxide hydrolase, and epoxyeicosatrienoic acids in metabolic diseases. Adv Nutr. 2016;7:1122–8.
Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes. 2003;52:1–8.
Pucci G, Alcidi R, Tap L, Battista F, Mattace-Raso F, Schillaci G. Sex- and gender-related prevalence, cardiovascular risk and therapeutic approach in metabolic syndrome: a review of the literature. Pharm Res. 2017;120:34–42.
Goldman R, Enewold L, Pellizzari E, Beach JB, Bowman ED, Krishnan SS, et al. Smoking increases carcinogenic polycyclic aromatic hydrocarbons in human lung tissue. Cancer Res. 2001;61:6367–71.
Gunter R, Szeto E, Jeong SH, Suh S, Waters AJ. Cigarette smoking in South Korea: a narrative review. Korean J Fam Med. 2020;41:3–13.
Sun K, Liu J, Ning G. Active smoking and risk of metabolic syndrome: a meta-analysis of prospective studies. PLoS One. 2012;7:e47791.
Wang J, Bai Y, Zeng Z, Wang J, Wang P, Zhao Y, et al. Association between life-course cigarette smoking and metabolic syndrome: a discovery-replication strategy. Diabetol Metab Syndr. 2022;14:11.
Damasceno DC, Sinzato YK, Bueno A, Dallaqua B, Lima PH, Calderon IM, et al. Metabolic profile and genotoxicity in obese rats exposed to cigarette smoke. Obesity. 2013;21:1596–601.
Kuang D, Zhang W, Deng Q, Zhang X, Huang K, Guan L, et al. Dose-response relationships of polycyclic aromatic hydrocarbons exposure and oxidative damage to DNA and lipid in coke oven workers. Environ Sci Technol. 2013;47:7446–56.
Shimada T, Fujii-Kuriyama Y. Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1. Cancer Sci. 2004;95:1–6.
O’Malley M, King AN, Conte M, Ellingrod VL, Ramnath N. Effects of cigarette smoking on metabolism and effectiveness of systemic therapy for lung cancer. J Thorac Oncol. 2014;9:917–26.
Parascandola M, Xiao L. Tobacco and the lung cancer epidemic in China. Transl Lung Cancer Res. 2019;8:S21–S30.
Rey-Salgueiro L, Garcia-Falcon MS, Martinez-Carballo E, Simal-Gandara J. Effects of toasting procedures on the levels of polycyclic aromatic hydrocarbons in toasted bread. Food Chem. 2008;108:607–15.
Acknowledgements
This study used data from the KNHANES study, which was supported by the Institutional Review Board of the Korea Centers for Disease Control and Prevention (KCDC). This research also was supported by a grant (20162MFDS112) from the Ministry of Food and Drug Safety in 2020.
Funding
This research was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No.2020R1C1C1014286). MSIT: Ministry of Science and ICT.
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SS conceived and designed the study, acquired data, and played an important role in interpreting the results. JZ was responsible for extracting and analyzing data, interpreting results, and drafting of the manuscript. L-JT, HJ, JJ, J-YL, GL, and SP played an important role in acquiring the data. B-KM and KC revised the manuscript. All authors reviewed the manuscript.
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The present study complied with the principles of the Declaration of Helsinki and the study protocols for the KNHANES VI and VII were approved by the Institutional Review Board of the Korea Centers for Disease Control and Prevention (KCDC) (IRB no. 2013-07CON-03-4C, 2013-12EXP-03-5C, 2018-01-03-P-A).
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Zhang, J., Tan, LJ., Jung, H. et al. Association of smoking and dietary polycyclic aromatic hydrocarbon exposure on the prevalence of metabolic syndrome in Korean adults. J Expo Sci Environ Epidemiol 33, 831–839 (2023). https://doi.org/10.1038/s41370-023-00541-1
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DOI: https://doi.org/10.1038/s41370-023-00541-1