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Formation of amino-imidazo-azaarenes and carbolines in fried beef patties and chicken breasts under different cooking conditions in Korea

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Abstract

The effect of cooking temperature and time on amino-imidazo-azaarenes (AIAs) and carbolines in fried ground beef patties and chicken breast under different cooking conditions in Korea was evaluated. Beef patties were fried at different temperatures (150, 180, and 230°C) for 4, 8, 12, and 16 min per each side and then the amount of AIAs and carbolines was evaluated by solid-phase extraction and HPLC-MS analysis. In fried ground beef patties, formations of 9H-pyrido [3,4-b]indole (Norharman) and 1-methyl-9H-pyrido [3,4-b]indole (Harman) were dramatically increased at 230°C for 16 min. Concentrations of Norhanrman and Harman formed at 230°C for 16 min/side were 12 and 40 times greater than level those of Norharman formed at same cooking condition. In fried chicken breasts, 2-amino-3,7,8-trimethylimidazo[4,5-f] quinoxaline (7,8-DiMeIQx) and 2-amino-3,4,7,8-tetramethylimidazo[ 4,5-f]quinoxaline (Tri-MeIQx) were not found at 150 and 180°C. Norhanrman formed at 230°C for 16 min was approximately 4 times higher than fried chicken breasts at 180°C. These results suggest that increase of cooking temperature and time was directly affected on AIAs and carbolines formation in Korean cooked meat.

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References

  1. Skog KI, Johansson MAE, Jägerstad MI. Carcinogenic heterocyclic amines in model systems and cooked foods: A review on formation, occurrence, and intake. Food Chem. Toxicol. 36: 879–896 (1998)

    Article  CAS  Google Scholar 

  2. Sinha R, Knize MG, Salmon CP, Brown ED, Rhodes D, Felton JS, Levander OA, Rothman N. Heterocyclic amine content of pork products cooked by different methods and to varying degrees of doneness. Food Chem. Toxicol. 36: 289–297 (1998)

    Article  CAS  Google Scholar 

  3. Sugimura T. Nutrition and dietary carcinogens. Carcinogenesis 21: 387–395 (2000)

    Article  CAS  Google Scholar 

  4. Skog K, Solyakov A. Heterocyclic amines in poultry products: A literature review. Food Chem. Toxicol. 40: 1213–1221 (2002)

    Article  CAS  Google Scholar 

  5. Skog K. Problems associated with the determination of heterocyclic amines in cooked foods and human exposure. Food Chem. Toxicol. 40: 1197–1203 (2002)

    Article  CAS  Google Scholar 

  6. Solyakov A, Skog K. Screening for heterocyclic amines in chicken cooked in various ways. Food Chem. Toxicol. 40: 1205–1211 (2002)

    Article  CAS  Google Scholar 

  7. Ito N, Hasegawa R, Sano M, Tamano S, Esumi H, Takayama S, Sugimura T. A new colon and mammary carcinogen in cooked food, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Carcinogenesis 12: 1503–1506 (1991)

    Article  CAS  Google Scholar 

  8. Hagiwara A, Tanaka H, Kurata Y, Kato T, Tsuda H, Ito N. Lack of hepatotoxicity or promotion of enzyme-altered liver foci development in rats treated with harman or norharman. J. Toxicol. Env. Heal. A 29: 211–218 (1990)

    Article  CAS  Google Scholar 

  9. Wakabayashi K, Totsuka Y, Fukutome K, Oguri A, Ushiyama H, Sugimura T. Human exposure to mutagenic/carcinogenic heterocyclic amines and comutagenic/fb-carbolines. Mutat. Res. 376: 253–259 (1997)

    CAS  Google Scholar 

  10. Ryu DY, Pratt VS, Davis CD, Schut HA, Snyderwine EG. In vivo mutagenicity and hepatocarcinogenicity of 2-amino-3,8-dimethylimidazo(4,5-f)quinoxaline (MeIQx) in bitransgenic c-myc/lambda-lacz mice. Cancer Res. 59: 2587–2592 (1999)

    CAS  Google Scholar 

  11. Imaida K, Sano M, Tamano S, Asamoto M, Ogawa K, Futakuch IM, Shirai T. Organ dependent enhancement of rat 3,20-dimethyl-4-aminobiphenyl (DMAB) carcinogenesis by 2-amino-1-methyl-6-phenylimidazo(4,5-b)pyridine (PhIP)-Positive effects on the intestine but not the prostate. Carcinogenesis 22: 1295–1299 (2001)

    Article  CAS  Google Scholar 

  12. IARC. Some natural occurring substances: Food items and constituents heterocyclic amines and mycotoxins. IARC Monogr. Eval. Carc. 56: 165–231 (2003)

    Google Scholar 

  13. Jägerstad M, Laser-Reuterswärd A, Öste R, Dahlqvist A, Grivas S, Olsson K, Nyhammar T. Creatinine and Maillard reaction products as precursors of mutagenic compounds formed in fried beef. pp. 507–519. In: The Maillard Reaction in Foods and Nutrition. Waller GR, Feather MS (eds). American Chemical Society, Washington, DC, USA (1983)

    Chapter  Google Scholar 

  14. Chiu CP, Yang DJ, Chen BH. Formation of heterocyclic amines in cooked chicken legs. J. Food Protect. 61: 712–719 (1998)

    CAS  Google Scholar 

  15. Chen BH, Lee KH, Tai CY. Formation of heterocyclic amines in fried fish fiber during processing and storage. J. Food Protect. 63: 1415–1420 (2000)

    CAS  Google Scholar 

  16. Sinha R, Rothman N, Brown ED, Salmon CP, Knize MG, Swanson CA, Rossi SC, Mark SD, Levander OA, Felton JS. High concentrations of the carcinogen 2-amino-1-methyl-6-phenylimidazo-[4,5-b] pyridine (PhIP) occur in chicken but are dependent on the cooking method. Cancer Res. 55: 4516–4519 (1995)

    CAS  Google Scholar 

  17. Holder CL, Preece SW, Conway SC, Pu YM, Doerge DR. Quantification of heterocyclic amine carcinogens in cooked meats using isotope dilution liquid chromatography/atmospheric pressure chemical ionization tandem mass spectrometry. Rapid Commun. Mass Sp. 11: 1667–1672 (1997)

    Article  CAS  Google Scholar 

  18. Knize MG, Salmon CP, Hopmans EC, Felton JS. Analysis of foods for heterocyclic aromatic amine carcinogens by solidphase extraction and high-performance liquid chromatography. J. Chromatogr. A 763: 179–185 (1997)

    Article  CAS  Google Scholar 

  19. Salmon CP, Knize MG, Felton JS. Effects of marinating on heterocyclic amine carcinogen formation in grilled chicken. Food Chem. Toxicol. 35: 433–441 (1997)

    Article  CAS  Google Scholar 

  20. Knize MG, Andresen BD, Healy SK, Shen NH, Lewis PR, Bjeldanes LF, Hatch FT, Felton JS. Effect of temperature, patty thickness, and fat content on the production of mutagens in fried ground beef. Food Chem. Toxicol. 23: 1035–1040 (1985)

    Article  CAS  Google Scholar 

  21. Jung J, Koo WW. Demand for meat and fish products in Korea. 2002 Annual Meeting, July 28–31, Long Beach, CA, USA. Agricultural and Applied Economics Association, Milwaukee, WI, USA (2002)

    Google Scholar 

  22. Hermann S, Linseisen J, Chang-Claude J. Nutrition and breast cancer risk by age 50: A population-based case-control study in Germany. Nutr. Cancer 44: 23–34 (2002)

    Article  Google Scholar 

  23. Cho E, Chen WY, Hunter DJ, Stampfer MJ, Colditz GA, Hankinson SE, Willett WC. Red meat intake and risk of breast cancer among premenopausal women. Arch. Intern. Med. 166: 2253–2259 (2006)

    Article  Google Scholar 

  24. Taylor EF, Burley VJ, Greenwood DC, Cade JE. Meat consumption and risk of breast cancer in the UK women’s cohort study. Brit. J. Cancer. 96: 1139–1146 (2007)

    Article  CAS  Google Scholar 

  25. Missmer SA, Smith-Warner SA, Spiegelman D, Yaun SS, Adami HO, Beeson WL, van den Brandt PA, Fraser GE, Freudenheim JL, Goldbohm RA, Graham S, Kushi LH, Miller AB, Potter JD, Rohan TE, Speizer FE, Toniolo P, Willett WC, Wolk A, Zeleniuch-Jacquotte A, Hunter DJ. Meat and dairy food consumption and breast cancer: A pooled analysis of cohort studies. Int. J. Epidemiol. 31: 78–85 (2002)

    Article  Google Scholar 

  26. Gross GA, Gruter A. Quantitation of mutagenic/carcinogenic heterocyclic amines in food products. J. Chromatogr. A 592: 271–278 (1992)

    Article  CAS  Google Scholar 

  27. Balogh Z, Gray JI. Formation and inhibition of heterocyclic aromatic amines in fried ground beef patties. Food Chem. Toxicol. 38: 395–401 (2000)

    Article  CAS  Google Scholar 

  28. Bordas M, Moyano E, Puignou L, Galceran MT. Formation and stability of heterocyclic amines in a meat flavour model system: Effect of temperature, time, and precursors. J. Chromatogr. B 802: 11–17 (2004)

    Article  CAS  Google Scholar 

  29. Knize MG, Dolbeare FA, Carroll KL, Moore DH 2nd, Felton JS. Effect of cooking time and temperature on the heterocyclic amine content of fried beef patties. Food Chem. Toxicol. 32: 595–603 (1994)

    Article  CAS  Google Scholar 

  30. Abdulkarim BG, Smith JS. Heterocyclic amines in fresh and processed meat products. J. Agr. Food Chem. 46: 4680–4687 (1998)

    Article  CAS  Google Scholar 

  31. Busquets R, Bordas M, Toribio F, Puignou L, Galceran MT. Occurrence of heterocyclic amines in several home-cooked meat dishes of the Spanish diet. J. Chromatogr. B 802: 79–86 (2004)

    Article  CAS  Google Scholar 

  32. Louis ED, Zheng W, Jiang W, Bogen KT, Keating GA. Quantification of the neurotoxic β-carboline harmane in barbecued/grilled meat samples and correlation with level of doneness. J. Toxicol. Env. Heal. A 70: 1014–1019 (2007)

    Article  CAS  Google Scholar 

  33. Pais P, Knize MG. Chromatographic and related techniques for the determination of aromatic heterocyclic amines in foods. J. Chromatogr. B 747: 139–169 (2000)

    Article  CAS  Google Scholar 

  34. Galceran MT, Pais P, Puignou L. Isolation by solid-phase extraction and liquid chromatographic determination of mutagenic amines in beef extracts. J. Chromatogr. A 719: 203–212 (1996)

    Article  CAS  Google Scholar 

  35. Sinha R, Rothman N, Brown ED, Mark SD, Hoover RN, Caporaso NE, Levander OA, Knize MG, Lang NP, Kadlubar FF. Pan-fried meat containing high levels of heterocyclic aromatic amines but low levels of polycyclic aromatic hydrocarbons induces cytochrome P4501A2 activity in humans. Cancer Res. 54: 6154–6159 (1994)

    CAS  Google Scholar 

  36. Back YM, Lee JH, Shin HS, Lee KG. Analysis of heterocyclic amines and β-carbolines by liquid chromatography-mass spectrometry in cooked meats commonly consumed in Korea. Food Addit. Contam. 26: 298–305 (2009)

    Article  CAS  Google Scholar 

  37. Brockstedt U, Pfau W. Formation of 2-amino-a-carbolines in panfried poultry and 32P-postlabelling analysis of DNA adducts. Z. Lebensm. Unters. For. 207: 472–476 (1998)

    Article  CAS  Google Scholar 

  38. Knize MG, Dolbeare FA, Cunningham PL, Felton JS. Mutagenic activity and heterocyclic amine content of the human diet. pp. 30–38. In: Heterocyclic Amines in Cooked Foods: Possible Human Carcinogens. Adamson HA, Gustafsson J, Ito N, Nagao M, Sugimura T, Wakabayashi K, Yamazoe Y (eds). Princeton Scientific Publishing, Princeton, NJ, USA (1995)

    Google Scholar 

  39. Felton JS, Fultz E, Dolbeare FA, Knize MG. Effect of microwave pretreatment on heterocyclic aromatic amine mutagens/carcinogens in fried beef patties. Food Chem. Toxicol. 32: 897–903 (1994)

    Article  CAS  Google Scholar 

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Dong, A., Lee, J. & Shin, HS. Formation of amino-imidazo-azaarenes and carbolines in fried beef patties and chicken breasts under different cooking conditions in Korea. Food Sci Biotechnol 20, 735–741 (2011). https://doi.org/10.1007/s10068-011-0103-9

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  • DOI: https://doi.org/10.1007/s10068-011-0103-9

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