Abstract
Data from National Health and Nutrition Examination Survey for US population aged ≥ 6 years for 2013–2014 were used to analyze data for four heterocyclic aromatic amines (HCAA), namely 2-amino-9H-pyrido[2,3-b]indole (AαC), 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhlP), harman, and norharman. Data were analyzed separately for children aged 6–11 years (N = 416), adolescents aged 12–19 years (N = 475), adults aged 20–64 years (N = 1913), and seniors aged ≥ 65 years (N = 458). Adult males had lower concentrations of AαC and harman than adult females (1.44 vs. 2.22 pg/mL for AαC, p < 0.01 and 136.8 vs. 163.2 pg/mL for harman, p = 0.04). Racial/ethnic differences were observed in the adjusted concentrations of HCAAs. For adults, adjusted concentrations of HCAAs were lower for non-Hispanic Asians and Hispanics as compared to non-Hispanic blacks and whites. For example for AαC, the adjusted concentrations for non-Hispanic Asians, Hispanics, non-Hispanic blacks and whites were 1.16, 2.00, 2.37, and 2.16 pg/mL respectively. Adjusted concentrations of AαC were found to be lower among nonsmokers as compared to smokers for adolescents (0.34 vs. 1.32 pg/mL, p < 0.01), adults (0.40 vs. 7.91 pg/mL, p < 0.01), and seniors (0.30 vs. 4.29 pg/mL, p < 0.01). For both harman and norharman, adult nonsmokers had lower adjusted concentrations than smokers (125.7 vs. 177.6 pg/mL, p < 0.01 for harman, 296.1 vs. 421.6 pg/mL, p < 001, for norharman). Exposure to environmental tobacco smoke was found to be associated with higher concentrations of AαC among adolescents (p = 0.01) and adults (p = 0.01) and for harman (p = 0.01) and norharman (p = 0.01) among seniors. In conclusion, concentrations of selected HCAAs can be several fold higher among smokers as compared to nonsmokers and gender as well as race/ethnicity also affect the observed concentrations of HCAA.






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References
Carrizo D, Brennan SF, Chevallier OP, Woodside J, Cooper KM, Cantwell MM, Cuskelly G, Elliott CT (2017) Distribution of serum levels of persistent organic pollutants, heterocyclic aromatic amine theoretical intake and nutritional cofactors in a semi-rural island population. Environ Sci Pollut Res Int 24:22393–22401. https://doi.org/10.1007/s11356-017-9851-2
Chiang VS, Quek SY (2017) The relationship of red meat with cancer: effects of thermal processing and related physiological mechanisms. Crit Rev Food Sci Nutr 57(6):1153–1173. https://doi.org/10.1080/10408398.2014.967833
Demeyer D, Mertens B, De Smet S, Ulens M (2016) Mechanisms linking colorectal cancer to the consumption of (processed) red meat: a review. Crit Rev Food Sci Nutr 56(16):2747–2766. https://doi.org/10.1080/10408398.2013.873886
Fu Y, Zhao G, Wang S, Yu J, Xie F, Wang H, Xie J (2014) Simultaneous determination of fifteen heterocyclic aromatic amines in the urine of smokers and nonsmokers using ultra-high performance liquid chromatography-tandem mass spectrometry. J Chromatogr A 1333:45–53
García-Lomillo J, Viegas O, Gonzalez-SanJose ML, Ferreira IM (2017) Influence of red wine pomace seasoning and high-oxygen atmosphere storage on carcinogens formation in barbecued beef patties. Meat Sci 125:10–15. https://doi.org/10.1016/j.meatsci.2016.11.009
Gibis M, Weiss J (2017) Inhibitory effect of cellulose fibers on the formation of heterocyclic aromatic amines in grilled beef patties. Food Chem 229:828–836. https://doi.org/10.1016/j.foodchem.2017.02.130
Jeyakumar A, Dissabandara L, Gopalan V (2017) A critical overview on the biological and molecular features of red and processed meat in colorectal carcinogenesis. J Gastroenterol 52(4):407–418. https://doi.org/10.1007/s00535-016-1294-x
Konorev D, Koopmeiners JS, Tang Y, Thompson EAF, Jensen JA, Hatsukami DK, Turesky RJ (2015) Measurement of the heterocyclic amines 2-amino-9H-pyrido[2,3-b]indole and 2-amino-1-methyl-6-phnyimidao[4,5-b]pyridine in urine: effects of cigarette smoking. Chem Res Toxicol 28:2390–2399. https://doi.org/10.1021/acs.chemrestox.5b00401
Le Marchand L, Yonemori K, White KK, Franke AA, Wilkens LR, Turesky RJ (2016) Dose validation of PhIP hair level as a biomarker of heterocyclic aromatic amines exposure: a feeding study. Carcinogenesis 37(7):685–691. https://doi.org/10.1093/carcin/bgw049
Lubin JH, Colt JS, Camann D, Davis S, Cerhan JR, Severson RK, Bernstein L, Hartge P (2004) Epidemiologic evaluation of measurement data in the presence of detection limits. Environ Health Perspect 112(17):1691–1696
Roemer E, Meisgen T, Diekmann J, Conroy L, Stabbert R (2016) Heterocyclic aromatic amines and their contribution to the bacterial mutagenicity of the particulate phase of cigarette smoke. Toxicol Lett 243:40–47. https://doi.org/10.1016/j.toxlet.2015.12.008
Rohrmann S, Nimptsch K, Sinha R, Willett WC, Giovannucci EL, Platz EA, Wu K (2015) Intake of meat mutagens and risk of prostate Cancer in a cohort of U.S. health professionals. Cancer Epidemiol Biomark Prev 24(10):1557–1563. https://doi.org/10.1158/1055-9965.EPI-15-0068-T.
Sabally K, Sleno L, Jauffrit JA, Iskandar MM, Kubow S (2016) Inhibitory effects of apple peel polyphenol extract on the formation of heterocyclicamines in pan fried beef patties. Meat Sci 117:57–62. https://doi.org/10.1016/j.meatsci.2016.02.040
Soladoye OP, Shand P, Dugan MER, Gariépy C, Aalhus JL, Estévez M, Juárez M (2017) Influence of cooking methods and storage time on lipid and protein oxidation and heterocyclic aromatic amines production in bacon. Food Res Int 99(Pt 1):660–669. https://doi.org/10.1016/j.foodres.2017.06.029.
Tengilimoglu-Metin MM, Kizil M (2017) Reducing effect of artichoke extract on heterocyclic aromatic amine formation in beef and chicken breast meat. Meat Sci 134:68–75. https://doi.org/10.1016/j.meatsci.2017.07.018
Tengilimoglu-Metin MM, Hamzalioglu A, Gokmen V, Kizil M (2017) Inhibitory effect of hawthorn extract on heterocyclic aromatic amine formation in beef and chicken breast meat. Food Res Int 99(Pt 1):586–595. https://doi.org/10.1016/j.foodres.2017.06.044.
Turesky RJ (2002) Heterocyclic aromatic amine metabolism, DNA adduct formation, mutagenesis, and carcinogenesis. Drug Metab Rev 34(3):625–650
Unal K, Karakaya M, Oz F (2017) The effects of different spices and fat types on the formation of heterocyclic aromatic amines in barbecued sucuk. J Sci Food Agric 98:719–725. https://doi.org/10.1002/jsfa.8519
Wang P, Hong Y, Ke W, Hu X, Chen F (2017) Formation of heterocyclic amines in Chinese marinated meat: effects of animal species and ingredients (rock candy, soy sauce and rice wine). J Sci Food Agric 97(12):3967–3978. https://doi.org/10.1002/jsfa.8259
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Jain, R.B. Concentrations of selected heterocyclic aromatic amines among US population aged ≥ 6 years: data from NHANES 2013–2014. Environ Sci Pollut Res 25, 19859–19874 (2018). https://doi.org/10.1007/s11356-018-2210-0
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DOI: https://doi.org/10.1007/s11356-018-2210-0


