Cooking with elaborate recipes can reduce the formation of mutagenic heterocyclic amines and promote co-mutagenic amines

References

• Alaejos MS, González V, Afonso AM. 2008. Exposure to heterocyclic aromatic amines from the consumption of cooked red meat and its effect on human cancer risk: a review. Food Addit Contam Part A. 25:2–24.
   Web of Science ®Google Scholar
• Bellamri M, Xiao S, Murugan P, Weight CJ, Turesky RJ. 2018. Metabolic activation of the cooked meat carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine in human prostate. Toxicol Sci. 63:543–556.
   Google Scholar
• Bermudo E, Buquets R, Barcelo-Barrachina E, Puignou L, FJ Santos, Galceran MT. 2004. Preparation of a beef-extract as a laboratory reference material for the determination of heterocyclic amines. J. Chromatogr B. 802:61–68.
   PubMed Web of Science ®Google Scholar
• Borgen E, Skog K. 2004. Heterocyclic amines in some Swedish cooked foods industrially prepared or from fast food outlets and restaurants. Mol Nutr Food Res. 48:292–298.
   PubMed Web of Science ®Google Scholar
• Busquets R. 2012. Food borne carcinogens: a dead end? In: Pesheva M, Dimitrov M, Stoycheva TS, editors. Carcinogen. 1 ed. Rijeka (Croatia): InTech; p. 184.
   Google Scholar
• Busquets R, Bordas M, Toribio F, Puignou L, Galceran MT. 2004. Occurrence of heterocyclic amines in several home-cooked meat dishes of the Spanish diet. J Chromatogr B. 802:79–86.
   PubMed Web of Science ®Google Scholar
• Busquets R, Puignou L, Galceran MT, Skog K. 2006. Effect of red wine marinades on the formation of heterocyclic amines in fried chicken breast. J Agric Food Chem. 54:8376–8384.
   PubMed Web of Science ®Google Scholar
• Cruz-Hernandez A, Agim ZS, Montenegro PC, McCabe GP, Rochet JC, Cannon JR. 2018. Selective dopaminergic neurotoxicity of three heterocyclic amine subclasses in primary rat midbrain neurons. Neurotoxicology. 65:68–84.
   PubMed Web of Science ®Google Scholar
• Gibis M. 2007. Effect of oil marinades with garlic, onion, and lemon juice on the formation of heterocyclic aromatic amines in fried beef patties. J Agric Food Chem. 55:10240–10247.
   PubMed Web of Science ®Google Scholar
• Gibis M. 2016. Heterocyclic aromatic amines in cooked meat products: causes, formation, occurrence, and risk assessment. Compr Rev Food Sci Food Saf. 15:269–302.
   PubMed Web of Science ®Google Scholar
• Gibis M, Weiss J. 2012. Antioxidant capacity and inhibitory effect of grape seed and rosemary extract in marinades on the formation of heterocyclic amines in fried beef patties. Food Chem. 134:766–774.
   PubMed Web of Science ®Google Scholar
• Herraiz T. 2000. Tetrahydro-beta-carboline-3-carboxylic acid compounds in fish and meat: possible precursors of co-mutagenic beta-carbolines norharman and harman in cooked foods. Food Addit Contam. 17:859–866.
   PubMed Web of Science ®Google Scholar
• Herraiz T. 2002. Identification and occurrence of the bioactive β-carbolines norharman and harman in coffee brews. Food Addit Contam. 19(8):748–754.
   PubMed Web of Science ®Google Scholar
• Herraiz T. 2004. Relative exposure to β-carbolines norharman and harman from foods and tobacco smoke. Food Addit Contam. 21:1041–1050.
   PubMedGoogle Scholar
• Herraiz T. 2016. N-methyltetrahydropyridines and pyridinium cations as toxins and comparison with naturally-occurring alkaloids. Food Chem Toxicol. 97:23–39.
   PubMed Web of Science ®Google Scholar
• [IARC] International Agency for Research on Cancer. 1993. Some natural occurring substances: food items and constituents. Heterocyclic amines and mycotoxins. IARC Monogr Eval Carcinog Risks Chem Hum. 56:163–242.
   Google Scholar
• Ho V, Peacock S, Massey TE, Godschalk RWL, van Schooten FJ, Chen J, King WD. 2015. Gene–diet interactions in exposure to heterocyclic aromatic amines and bulky DNA adduct levels in blood leukocytes. Environ Mol Mutagen. 56:609–620.
   PubMed Web of Science ®Google Scholar
• Iwasaki M, Kataoka H, Ishihara J, Takachi R, Hamada GS, Sharma S, Marchand LL, Tsugane S. 2010. Heterocyclic amines content of meat and fish cooked by Brazilian methods. J Food Compos Anal. 23:61–69.
   PubMed Web of Science ®Google Scholar
• Jägerstad M, Skog K, Arvidsson P, Solyakov A. 1998. Chemistry, formation and occurrence of genotoxic heterocyclic amines identified in model systems and cooked foods. Z Lebensm Unters Forsch. 207:419–427.
   Google Scholar
• Jinap S, Hasnol NDS, Sanny M, Jahurul MHA. 2018. Effect of organic acid ingredients in marinades containing different types of sugar on the formation of heterocyclic amines in grilled chicken. Food Cont. 84:478–484.
   Web of Science ®Google Scholar
• Khan MR. 2015. Influence of food condiments on the formation of carcinogenic heterocyclic amines in cooked chicken and determination by LC–MS/MS. Food Addit Contam Part A. 32:307–314.
   PubMed Web of Science ®Google Scholar
• Khan MR, Bertus LM, Busquets R, Puignou L. 2009b. Mutagenic heterocyclic amine content in thermally processed offal products. Food Chem. 112:838–843.
   Web of Science ®Google Scholar
• Khan MR, Busquets R, Saurina J, Hernández S, Puignou L. 2013. Identification of seafood as an important dietary source of heterocyclic amines by chemometry and chromatography mass spectrometry. Chem Res Toxicol. 26:1014–1022.
   PubMed Web of Science ®Google Scholar
• Khan MR, Mila A, Busquets R, Santos FJ, Puignou L. 2009a. Preparation and characterisation of fried chicken as a laboratory reference material for the analysis of heterocyclic amines. J Chromatogr B. 877:1997–2002.
   PubMed Web of Science ®Google Scholar
• Khan MR, Naushad M, Alothman ZA. 2017. Presence of heterocyclic amine carcinogens in home-cooked and fast-food camel meat burgers commonly consumed in Saudi Arabia. Sci Rep. 7:1–7.
   PubMed Web of Science ®Google Scholar
• Louis ID, Zheng W, Jiang W, Bogen KT, Keating GA. 2007. Quantification of the neurotoxic β-carboline harmane in barbecued/grilled meat samples and correlation with level of doneness. J Toxicol Environ Health. 70:1014–1019.
   PubMed Web of Science ®Google Scholar
• Mendel J. 1997. Cooking in Spain. edition 1 ed. S.L. (Spain): Ediciones Santana; p. 376.
   Google Scholar
• Murkovic M, Hj W, Geiszler S, Fröhlich K, Pfannhauser W. 1999. Formation of the food associated carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in model systems. Food Chem. 65:233–237.
   Web of Science ®Google Scholar
• [NTP] National Toxicology Program. 2016. US. 14th Report on Carcinogens, National Toxicology Program, https://ntp.niehs.nih.gov/pubhealth/roc/index-1.html (Accessed 2018 Aug 21)
   Google Scholar
• Murkovic M, Steinberger D, Pfannhauser W. 1998. Antioxidant spices reduce the formation of heterocyclic amines in fried meat. Z Lebensm Unters Forsch. 207:477–480.
   Google Scholar
• Oz F, Mo Y. 2017. The effects of different cooking methods on the formation of heterocyclic aromatic amines in turkey meat. J Food Process Preserv. 41:e13196–e13204.
   Web of Science ®Google Scholar
• Pathak KV, Chiu TL, Amin EA, Turesky RJ. 2016. Methemoglobin formation and characterization of hemoglobin adducts of carcinogenic aromatic amines and heterocyclic aromatic amines. Chem Res Toxicol. 29:255–269.
   PubMed Web of Science ®Google Scholar
• Persson E, Sjöholm I, Skog K. 2006. Effect of high water-holding capacity on the formation of heterocyclic amines in fried beefburgers. J Agric Food Chem. 51:4472–4477.
   Google Scholar
• Pfau W, Skog K. 2004. Exposure to β-carbolines norharman and harman. J Chromatogr B. 802:115–126.
   PubMed Web of Science ®Google Scholar
• Rannou C, Laroque D, Renault E, Prost C, Sérot T. 2016. Mitigation strategies of acrylamide, furans, heterocyclic amines and browning during the Maillard reaction in foods. Food Res Int. 90:154–176.
   PubMed Web of Science ®Google Scholar
• Rönner B, Lerche H, Bergmüller W, Freilinger C, Severin T, Pischetsrieder M. 2000. Formation of tetrahydro-β-carbolines and β-carbolines during the reaction of L-tryptophan with D-glucose. J Agric Food Chem. 48:2111–2116.
   PubMed Web of Science ®Google Scholar
• Sadrieh N, Davis CD. 1996. N-acetyltransferase expression and metabolic activation of the food-derived heterocyclic amines in the human mammary gland. Cancer Res. 56:2683–2687.
   PubMed Web of Science ®Google Scholar
• Salmon CP, Knize MG, Panteleakos FN, Wu RW, Nelson DO, Felton JS. 2000. Minimization of heterocyclic amines and thermal inactivation of Escherichia coli in fried ground beef. J Natl Cancer Inst. 92:1773–1778.
   PubMed Web of Science ®Google Scholar
• Santos FJ, Barceló-Barrachina E, Toribio F, Puignou L, Galceran MT, Persson E, Skog K, Messner C, Murkovic M, Nabinger U, et al. 2004. Analysis of heterocyclic amines in food products: interlaboratory studies. J Chromatogr B. 802:69–78.
   PubMed Web of Science ®Google Scholar
• Shabnam S, Jinap S, Alfi K, Mohd YAM, Ahmad FAR, Parvaneh H. 2018. Inhibitory effect of mixture herbs/spices on formation of heterocyclic amines and mutagenic activity of grilled beef. Food Addit Contam Part A. 1488085. doi:10.1080/19440049
   Google Scholar
• Sinha R, Rothman N, Brown ED, Salmon CP, Knize MG, Swanson CA, Rossi SC, Mark SD, Levander OA, Felton JS. 1995. 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.
   PubMed Web of Science ®Google Scholar
• Sinha R, Rothman N, Salmon CP, Knize MG, Brown ED, Swanson CA, Rhodes D, Rossi S, Felton JS, Levander OA. 1998. Heterocyclic amine content of beef cooked by different methods to varying degrees of doneness and gravy made from meat drippings. Food Chem Toxicol. 36:279–287.
   PubMed Web of Science ®Google Scholar
• Skog K, Johansson MAE, Jägerstad MI. 1998. Carcinogenic heterocyclic amines in model systems and cooked foods – a review on formation, occurrence and intake. Food Chem Toxicol. 36:879–896.
   PubMed Web of Science ®Google Scholar
• 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. 99:586–595.
   PubMed Web of Science ®Google Scholar
• Toribio F, Busquets R, Puignou L, Galceran MT. 2007. Heterocyclic amines in griddled beef steak analysed using a single extract clean-up procedure. Food Chem Toxicol. 45:667–675.
   PubMed Web of Science ®Google Scholar
• Turner ND, Lloyd SK. 2017. Association between red meat consumption and colon cancer: a systematic review of experimental results. Exp Biol Med. 242:813–839.
   PubMed Web of Science ®Google Scholar
• Viegas O, Amaro LF, Ferreira IM, Pinho O. 2012. Inhibitory effect of antioxidant-rich marinades on the formation of heterocyclic aromatic amines in pan-fried beef. J Agric Food Chem. 60:6235–6240.
   PubMed Web of Science ®Google Scholar
• Vitaglione P, Fogliano V. 2004. Use of antioxidants to minimize the human health risk associated to mutagenic/carcinogenic heterocyclic amines in food. J Chromatogr B. 802:189–199.
   PubMed Web of Science ®Google Scholar
• Zeng M, Li Y, He Z, Qin F, Chen J. 2016. Effect of phenolic compounds from spices consumed in China on heterocyclic amine profiles in roast beef patties by UPLC–MS/MS and multivariate analysis. Meat Sci. 116:50–57.
   PubMed Web of Science ®Google Scholar
• Zeng M, Zhang M, Chen J, He Z, Qin F, Hu C, Xu H, Tao G, Zhang S, Chen J. 2017. UPLC–MS/MS and multivariate analysis of inhibition of heterocyclic amine profiles by black pepper and piperine in roast beef patties. Chemom Intell Lab Syst. 168:96–106.
   Web of Science ®Google Scholar