Effects of smoke flavoring using different wood chips and barbecuing on the formation of polycyclic aromatic hydrocarbons and heterocyclic aromatic amines in salmon fillets

Autoři: Emel Oz aff001
Působiště autorů: Department of Food Engineering, Faculty of Agriculture, Ataturk University, Erzurum, Turkey aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227508


Herein, the concentrations of food toxicants, polycyclic aromatic hydrocarbons (PAHs) and heterocyclic aromatic amines (HAAs), in salmon fillets smoke flavored with different smoking wood chips (oak, apple, bourbon soaked oak, cherry and hickory) and barbecuing were determined. Benzo[a]anthracene (up to 0.24 ng/g) and chrysene (0.22 ng/g) were determined in the raw salmon fillets. While ∑PAH8 (benzo[a]anthracene, chrysene, benzo[b]fluoranthene, benzo[k]fluoranthene, benzo[a]pyrene, dibenzo[a,h]anthracene, benzo[g,h,i]perylene, indeno[1,2,3-cd]pyrene) in the raw samples ranged between 0.44 and 0.46 ng/g, smoke flavoring increased the amount of ∑PAH8 and the amount varied between 0.47 and 0.73 ng/g. Salmon smoked flavored with bourbon soaked oak, cherry and hickory wood chips and barbecued showed significantly (P <0.05) lower contents of ∑PAH4 (benzo[a]anthracene, chrysene, benzo[b]fluoranthene, benzo[a]pyrene) and ∑PAH8 compared to non-smoke flavored barbecued samples. Additionally, smoke flavoring with apple, bourbon soaked oak, and cherry wood chips significantly (P <0.05) reduced the total HAA contents in barbecued salmon. A remarkable result was that the bourbon-soaked oak and cherry wood chips had inhibitory effects on both PAH and HAA contents. In sum, barbecued non-smoke flavored and smoke flavored salmon with different wood chips could be considered safe from the perspective of the detected amounts of PAHs and HAAs in salmon fillets.

Klíčová slova:

Amines – Antioxidants – Fish – Meat – Salmon – Trout – Aromatic hydrocarbons – Carcinogens


1. Costa M, Viegas O, Melo A, Petisca C, Pinho O, Ferreira IM. Heterocyclic aromatic amine formation in barbecued sardines (Sardina pilchardus) and Atlantic salmon (Salmo salar). Journal of Agricultural and Food Chemistry, 2009; 57: 3173–3179. doi: 10.1021/jf8035808 19265446

2. Sidhu KS. Health benefits and potential risks related to consumption of fish or fish oil. Regulatory Toxicology and Pharmacology, 2003; 38: 336–344. doi: 10.1016/j.yrtph.2003.07.002 14623484

3. Stołyhwo A, Sikorski ZE. Polycyclic aromatic hydrocarbons in smoked fish–a critical review. Food Chemistry, 2005; 91: 303–311.

4. Stumpe-Vīksna I, Bartkevičs V, Kukāre A, Morozovs A. Polycyclic aromatic hydrocarbons in meat smoked with different types of wood. Food Chemistry, 2008; 110: 794–797.

5. Sun Y, Wu S, Gong G. Trends of research on polycyclic aromatic hydrocarbons in food: A 20-year perspective from 1997 to 2017. Trends in Food Science & Technology, 2018; 83: 86–98.

6. IARC (International Agency for Research on Cancer), Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Monographs on the evaluation of carcinogenic risks to humans, 2010; 92: 1. 21141735

7. Visciano P, Perugini M, Amorena M, Ianieri A. Polycyclic aromatic hydrocarbons in fresh and cold-smoked Atlantic salmon fillets. Journal of Food Protection, 2006; 69: 1134–1138. doi: 10.4315/0362-028x-69.5.1134 16715815

8. Moazzen M, Ahmadkhaniha R, Gorji MEh, Yunesian M, Rastkari N. Magnetic solid-phase extraction based on magnetic multi-walled carbon nanotubes for the determination of polycyclic aromatic hydrocarbons in grilled meat samples. Talanta, 2013; 115: 957–965. doi: 10.1016/j.talanta.2013.07.005 24054688

9. Phillips DH. Polycyclic aromatic hydrocarbons in the diet. Mutation research/genetic toxicology and environmental mutagenesis, 1999; 443: 139–147.

10. ur Rahman U, Sahar A, Khan MI, Nadeem M. Production of heterocyclic aromatic amines in meat: Chemistry, health risks and inhibition. A review. LWT-Food Science and Technology, 2014; 59: 229–233.

11. Nagao M, Honda M, Seino Y, Yahagi T, Sugimura T. Mutagenicities of smoked condensates and the charred surface of fish and meat. Cancer Letters, 1977; 2: 221–226. doi: 10.1016/s0304-3835(77)80025-6 45723

12. Oz F, Yuzer MO. The effects of cooking on wire and stone barbecue at different cooking levels on the formation of heterocyclic aromatic amines and polycyclic aromatic hydrocarbons in beef steak. Food Chemistry, 2016; 203: 59–66. doi: 10.1016/j.foodchem.2016.02.041 26948589

13. Duedahl-Olesen L, Aaslyng M, Meinert L, Christensen T, Jensen A, Binderup ML. Polycyclic aromatic hydrocarbons (PAH) in Danish barbecued meat. Food Control, 2015; 57: 169–176.

14. Forsberg ND, Stone D, Harding A, Harper B, Harris S, Matzke MM, et al. Effect of native American fish smoking methods on dietary exposure to polycyclic aromatic hydrocarbons and possible risks to human health. Journal of Agricultural and Food Chemistry, 2012; 60: 6899–6906. doi: 10.1021/jf300978m 22690788

15. Remy CC, Fleury M, Beauchêne J, Rivier M, Goli T. Analysis of PAH residues and amounts of phenols in fish smoked with woods traditionally used in French Guiana. Journal of Ethnobiology, 2016; 36: 312–326.

16. Farhadian A, Jinap S, Hanifah H, Zaidul I. Effects of meat preheating and wrapping on the levels of polycyclic aromatic hydrocarbons in charcoal-grilled meat. Food Chemistry, 2011; 124: 141–146.

17. Messner C, Murkovic M. Evaluation of a new model system for studying the formation of heterocyclic amines. Journal of Chromatography B, 2004; 802: 19–26.

18. Visciano P, Perugini M, Manera M, Amorena M. Selected polycyclic aromatic hydrocarbons in smoked tuna, swordfish and Atlantic salmon fillets. International Journal of Food Science & Technology, 2009; 44: 2028–2032.

19. Storelli M, Stuffler RG, Marcotrigiano G. Polycyclic aromatic hydrocarbons, polychlorinated biphenyls, chlorinated pesticides (DDTs), hexachlorocyclohexane, and hexachlorobenzene residues in smoked seafood. Journal of Food Protection, 2003; 66: 1095–1099. doi: 10.4315/0362-028x-66.6.1095 12801016

20. Zachara A, Gałkowska D, Juszczak L. Contamination of smoked meat and fish products from Polish market with polycyclic aromatic hydrocarbons. Food Control, 2017; 80: 45–51.

21. Rose M, Holland J, Dowding A, Petch SR, White S, Fernandes A, et al. Investigation into the formation of PAHs in foods prepared in the home to determine the effects of frying, grilling, barbecuing, toasting and roasting. Food and Chemical Toxicology, 2015; 78: 1–9. doi: 10.1016/j.fct.2014.12.018 25633345

22. Pöhlmann M, Hitzel A, Schwägele F, Speer K, Jira W. Influence of different smoke generation methods on the contents of polycyclic aromatic hydrocarbons (PAH) and phenolic substances in Frankfurter-type sausages. Food Control, 2013; 34: 347–355.

23. Malarut JA, Vangnai K. Influence of wood types on quality and carcinogenic polycyclic aromatic hydrocarbons (PAHs) of smoked sausages. Food Control, 2018; 85: 98–106.

24. Toth L, Potthast K. Chemical aspects of the smoking of meat and meat products. In Chichester C. O., Mrak E. M. K., & Schweigert B. S (Eds.). Advances in food research, New York: Academic Press, 1984; 87–158.

25. Stolyhwo A, Sikorski ZE. Polycyclic aromatic hydrocarbons in smoked fish. Food Chemistry, 2005; 91: 303–311.

26. European Commission E. Commission Regulation (EU) No 835/2011 of 19 August 2011 amending Regulation (EC) No 1881/2006 as regards maximum levels for polycyclic aromatic hydrocarbons in foodstuffs. Official Journal of the European Union, 2011; 215: 1–5.

27. Viegas O, Novo P, Pinto E, Pinho O, Ferreira I. Effect of charcoal types and grilling conditions on formation of heterocyclic aromatic amines (HAs) and polycyclic aromatic hydrocarbons (PAHs) in grilled muscle foods. Food and Chemical Toxicology, 2012; 50: 2128–2134. doi: 10.1016/j.fct.2012.03.051 22459130

28. Janoszka B. HPLC-fluorescence analysis of polycyclic aromatic hydrocarbons (PAHs) in pork meat and its gravy fried without additives and in the presence of onion and garlic. Food Chemistry, 2011; 126: 1344–1353.

29. Pais P, Salmon CP, Knize MG, Felton JS. Formation of mutagenic/carcinogenic heterocyclic amines in dry-heated model systems, meats, and meat drippings. Journal of Agricultural and Food Chemistry, 1999; 47: 1098–1108. doi: 10.1021/jf980644e 10552422

30. Skog K, Johansson M, Jägerstad M. Carcinogenic heterocyclic amines in model systems and cooked foods: a review on formation, occurrence and intake. Food and Chemical Toxicology, 1998; 36: 879–896. doi: 10.1016/s0278-6915(98)00061-1 9737435

31. Puangsombat K, Gadgil P, Houser TA, Hunt MC, Smith JS. Occurrence of heterocyclic amines in cooked meat products. Meat Science, 2012; 90: 739–746. doi: 10.1016/j.meatsci.2011.11.005 22129588

32. Oz F, Kotan G. Effects of different cooking methods and fat levels on the formation of heterocyclic aromatic amines in various fishes. Food Control, 2016; 67: 216–224.

33. Oz F, Kaya M. Heterocyclic aromatic amines in meat. Journal of Food Processing and Preservation, 2011; 35: 739–753.

34. Gross G, Grüter A. Quantitation of mutagegnic/carcinogenic heterocyclic aromatic amines in food products. Journal of Chromatography A, 1992; 592: 271–278.

35. Iwasaki M, Kataoka H, Ishihara J, Takachi R, Hamada GS, Sharma S, et al. Heterocyclic amines content of meat and fish cooked by Brazilian methods. Journal of Food Composition and Analysis, 2010; 23: 61–69. doi: 10.1016/j.jfca.2009.07.004 20383312

36. Oz F, Kaban G, Kaya M. Effects of cooking methods and levels on formation of heterocyclic aromatic amines in chicken and fish with Oasis extraction method. LWT-Food Science and Technology, 2010; 43: 1345–1350.

37. Oz E. Inhibitory effects of black cumin on the formation of heterocyclic aromatic amines in meatball. Plos One, 2019; 14: e0221680. doi: 10.1371/journal.pone.0221680 31454384

38. Murkovic M. Chemistry, formation and occurrence of genotoxic heterocyclic aromatic amines in fried products. European Journal of Lipid Science and Technology, 2004; 106: 777–785.

39. Vitaglione P, Fogliano V. Use of antioxidants to minimize the human health risk associated to mutagenic/carcinogenic heterocyclic amines in food. Journal of Chromatography B, 2004; 802: 189–199.

40. Britt C, Gomaa EA, Gray JI, Booren A.M. Influence of cherry tissue on lipid oxidation and heterocyclic aromatic amine formation in ground beef patties. Journal of Agricultural and Food Chemistry, 1998; 46: 4891–4897.

41. Weisburger JH, Nagao M, Wakabayashi K, Oguri A. Prevention of heterocyclic amine formation by tea and tea polyphenols. Cancer Letters, 1994; 83: 143–147. doi: 10.1016/0304-3835(94)90311-5 8062207

42. Kjallstrand J, Petersson G. Phenolic antioxidants in alder smoke during industrial maet curing. Food Chemistry, 2001; 74: 85–89.

43. Chiu C, Yang D, Chen B. Formation of heterocyclic amines in cooked chicken legs. Journal of Food Protection, 1998; 61: 712–719. doi: 10.4315/0362-028x-61.6.712 9709255

44. Skog K. Problems associated with the determination of heterocyclic amines in cooked foods and human exposure. Food and Chemical Toxicology, 2002; 40: 1197–1203. doi: 10.1016/s0278-6915(02)00052-2 12067584

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