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Association of smoking and dietary polycyclic aromatic hydrocarbon exposure on the prevalence of metabolic syndrome in Korean adults

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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Fig. 1: Flowchart of the selection.
Fig. 2: Adjusted prevalence ratios of MetS for different combinations of smoking status and PAH metabolite levels.

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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

  1. 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.

    Article  Google Scholar 

  2. Patel AB, Shaikh S, Jain KR, Desai C, Madamwar D. Polycyclic aromatic hydrocarbons: sources, toxicity, and remediation approaches. Front Microbiol. 2020;11:562813.

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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.

    Article  CAS  PubMed  Google Scholar 

  4. 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.

    Article  CAS  Google Scholar 

  5. Srogi K. Monitoring of environmental exposure to polycyclic aromatic hydrocarbons: a review. Environ Chem Lett. 2007;5:169–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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.

    Article  CAS  PubMed  Google Scholar 

  7. Huang PL. A comprehensive definition for metabolic syndrome. Dis Model Mech. 2009;2:231–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Borch-Johnsen K. The metabolic syndrome in a global perspective. The public health impact–secondary publication. Dan Med Bull. 2007;54:157–9.

    PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  10. 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.

  11. Le Magueresse-Battistoni B, Vidal H, Naville D. Environmental pollutants and metabolic disorders: the multi-exposure scenario of life. Front Endocrinol. 2018;9:582.

    Article  Google Scholar 

  12. Scinicariello F, Buser MC. Urinary polycyclic aromatic hydrocarbons and childhood obesity: NHANES (2001-2006). Environ Health Perspect. 2014;122:299–303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 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.

    Article  CAS  PubMed  Google Scholar 

  14. 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.

    Article  CAS  PubMed  Google Scholar 

  15. 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.

    Article  CAS  PubMed  Google Scholar 

  16. Lu L, Mackay DF, Pell JP. Meta-analysis of the association between cigarette smoking and peripheral arterial disease. Heart. 2014;100:414–23.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    Article  PubMed  Google Scholar 

  18. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  19. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  20. 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.

  21. 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.

    Article  CAS  PubMed  Google Scholar 

  22. 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.

    Article  CAS  PubMed  Google Scholar 

  23. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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.

    Article  CAS  Google Scholar 

  25. Humans IWGotEoCRt. Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Monogr Eval Carcinog Risks Hum. 2010;92:1–853.

    Google Scholar 

  26. 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.

    Article  CAS  PubMed  Google Scholar 

  27. 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.

  28. 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.

    Article  CAS  PubMed  Google Scholar 

  29. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nisbet IC, LaGoy PK. Toxic equivalency factors (TEFs) for polycyclic aromatic hydrocarbons (PAHs). Regul Toxicol Pharm. 1992;16:290–300.

    Article  CAS  Google Scholar 

  31. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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.

    Google Scholar 

  33. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 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.

    Article  PubMed  Google Scholar 

  35. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  36. 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.

    Article  CAS  PubMed  Google Scholar 

  37. 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.

    Article  CAS  Google Scholar 

  38. 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.

    Article  CAS  PubMed  Google Scholar 

  39. 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.

    Article  CAS  PubMed  Google Scholar 

  40. 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.

    PubMed  PubMed Central  Google Scholar 

  41. Schulz E, Anter E, Keaney JF Jr. Oxidative stress, antioxidants, and endothelial function. Curr Med Chem. 2004;11:1093–104.

    Article  CAS  PubMed  Google Scholar 

  42. Penning TM. Human aldo-keto reductases and the metabolic activation of polycyclic aromatic hydrocarbons. Chem Res Toxicol. 2014;27:1901–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Taddei S, Virdis A, Ghiadoni L, Sudano I, Salvetti A. Endothelial dysfunction in hypertension. J Cardiovasc Pharm. 2001;38:S11–4.

    Article  CAS  Google Scholar 

  44. Esser C, Rannug A. The aryl hydrocarbon receptor in barrier organ physiology, immunology, and toxicology. Pharm Rev. 2015;67:259–79.

    Article  CAS  PubMed  Google Scholar 

  45. 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.

    Article  Google Scholar 

  46. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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.

    Article  CAS  PubMed  Google Scholar 

  49. 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.

    Article  Google Scholar 

  50. 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.

    CAS  PubMed  Google Scholar 

  51. 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.

    Article  PubMed  Google Scholar 

  52. Sun K, Liu J, Ning G. Active smoking and risk of metabolic syndrome: a meta-analysis of prospective studies. PLoS One. 2012;7:e47791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  54. 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.

    Article  CAS  PubMed  Google Scholar 

  55. 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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  57. 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.

    Article  PubMed  Google Scholar 

  58. Parascandola M, Xiao L. Tobacco and the lung cancer epidemic in China. Transl Lung Cancer Res. 2019;8:S21–S30.

    Article  PubMed  PubMed Central  Google Scholar 

  59. 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.

    Article  CAS  PubMed  Google Scholar 

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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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Contributions

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.

Corresponding author

Correspondence to Sangah Shin.

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The authors declare no competing interests.

Ethical approval

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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