CC BY
10DOI: https://doi.org/10.21323/2414-438X-2022-7-4-282-287
Available online at https://www.meatjournal.ru/jour Original scientific article Open Access
MUTAGENIC AND/OR CARCINOGENIC COMPOUNDS A t d Reeived
Accepted in revised 06.12.2022
IN MEAT AND MEAT PRODUCTS: POLYCYCLIC Accepted or publication 10.12.2022
AROMATIC HYDROCARBONS PERSPECTIVE
Emel Oz
Ataturk University, Erzurum, Turkiye
Keywords: meat, thermal processes, polycyclic aromatic hydrocarbons, process parameters Abstract
Polycyclic aromatic hydrocarbons (PAHs) are widespread environmental contaminants posing a great risk to human health due to their mutagenic and/or carcinogenic properties. They are produced from incomplete combustion of a heat source, pyrolysis of organic components, and fat-induced flame formation. Meat and meat products are one of the major sources of PAH exposure. Since PAH intake increases the risk of cancer, understanding the factors affecting PAH formation in meat and meat products is very important within the scope of PAH exposure reduction strategies. In this study, the features and formation of PAHs, the factors affecting the formation of PAH compounds and their reduction/inhibition pathways were reviewed in order to provide a perspective on the presence of PAHs in meat and meat products.
For citation: Oz, E. (2022). Mutagenic and/or carcinogenic compounds in meat and meat products: polycyclic aromatic hydrocarbons perspective. Theory and Practice of Meat Processing, 7(4), 282-287. https://doi.org/10.21323/2414-438X-2022-7-4-282-287
Introduction
Polycyclic aromatic hydrocarbons (PAHs) are a large group of chemicals that contain 2-7 aromatic rings. PAHs are non-polar compounds of lipophilic nature [1,2,3]. They are formed through incomplete combustion or pyrolysis of organic matter [4]. Epidemiological studies have shown that PAH compounds can negatively affect the organism by interfering with the normal functioning of the cellular membrane and the enzyme system [5]. Storelli et al. [6] reported that PAHs bind to DNA and cause mutations that initiate the carcinogenic process. PAHs are considered common environmental pollutants due to their long-range transport and bioaccumulation [7]. Industrial emissions, agricultural resources, air, water, soil and foodstuffs are the main sources of PAHs [5]. However, it is reported that the most important PAH exposure source for humans is foodstuffs [7] and foodstuffs are responsible for approximately 88-98% of PAH pollution [8].
Early studies of PAHs focused on the analysis of industrial sources of PAHs. However, further studies have shown that environmental PAHs can be transferred to food such as fruits and vegetables, seafood, oils, etc [9,10]. On the other hand, food production processes based on high temperature application such as baking, frying and smoking also cause high levels of PAH formation [11,12]. Pyrolysis and oxidation of fat, protein and carbohydrates are induced during high temperature application, which can result in the production of high levels of PAHs. In addition, fat dripping onto the flame and returning to the meat as smoke can also lead to PAH production [2]. Considering
that meat with its rich protein and fat content is cooked by various methods before consumption, it is understood that cooked meat and meat products play an important role in PAH exposure through food. Especially, thermal processes such as smoking, grilling, barbecue, frying, roasting can cause high levels of PAH formation in meat due to high temperature, pyrolysis and intense smoke generation [8]. Indeed, it has been reported that meat and meat products contain high concentrations of PAH and are important sources for PAH exposure through foodstuffs [13,14].
Therefore, it is essential to understand the properties and occurrence of PAHs and the factors that influence PAH formation in order to develop strategies reducing exposure to PAHs, which have adverse health effects. The present review focuses on the features and formation of PAHs, the factors affecting the formation of PAH compounds in cooked meat and meat products and their reduction/inhibition pathways.
The structure, toxicity and health hazards of PAHs
PAH compounds exhibit toxic, mutagenic, and carcinogenic effects on humans [15]. They are easily absorbed by the body and can participate in metabolism due to their lipophilic nature [16]. In addition, PAHs can cause toxic-ity to organisms by interfering with the normal function of biological cell membranes and membrane-associated enzyme systems [17,18]. To date, approximately 160 different PAH compounds have been identified in nature and authorities such as the European Commission Scientific Committee on Food and the United States Environmental
Copyright © 2022, Oz E. This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/ by/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for any purpose, even commercially, provided the original work is properly cited and states its license.
Table 1. Some characteristics of individual PAHs used as markers in the assessment of PAH contamination
Compound name Abbreviation Molecule structure Chemical formula Molecular weight LARC classification* Genotoxity
Benz(a)anthracene BaA ¿CO C18H12 228.3 2B Positive
Chrysene Chry C18H12 228.3 2B Positive
Benzo(b)fluoranthene BbF C20H12 252.3 2B Positive
Benzo(a)pyrene BaP ofi? C20H12 252.3 1 Positive
* Carcinogenic; 2B: Possibly carcinogenic
Protection Agency have determined 16 of these compounds as priority contaminants, considering their mutagenic and carcinogenic properties [3,14]. Benzo[a]pyrene (BaP) is classified as a Group 1 carcinogen, while the majority of other high molecular weight PAHs are largely classified in Group 2A (probably carcinogenic to humans) or Group 2B (possibly carcinogenic to humans) [19] (Table 1).
Laboratory studies have revealed that prolonged exposure to PAH compounds causes lung cancer by inhalation, gastric cancer by ingestion with food, and skin cancer by contact, in animals [20,21]. Daniel et al. [22] declared that the risk of renal cell carcinoma increases with grilled meat consumption. Alomirah et al. [23] reported that the cancer risk associated with consumption of foods of animal origin by children/adolescents and adults is 2.63/107 and 9.3/107 BaP equivalents, respectively.
Several regulations have been declared to protect consumers against PAH intake from diet due to the negative effects of PAHs on health [24]. In this context, Benzo(a) pyrene (BaP) and ZPAH4 [BaP, Chrysene (Chry), Benz[a] anthracene (BaA) and Benzo[b]fluoranthene (BbF)] have been used as markers for the PAH contamination in food [25]. The legal limits of BaP and ZPAH4 were determined as 5 |g/kg and 30|g/kg for heat treated meat products, respectively [26].
Factors affecting the formation of PAH
compounds in meat and meat products
Many factors such as cooking method, cooking duration and distance, heat source and fuel type, direct/indirect heat application, pre-cooking processes and fat content of meat affect the formation of PAH compounds in meat and meat products (Figure 1).
Frying, grilling, baking, smoking, steaming are techniques commonly used in cooking of meat and meat products [2,24]. There is a strong correlation between PAH formation in meat and cooking methods. On the other hand, the level of PAHs formed varies widely depending on the cooking method [27,28,29,30]. In a study examining the effects of different cooking methods on PAH formation in beef, it was reported that the BaP and ZPAH4 content were lower in pan-fried samples compared to barbecue-cooked samples [31]. Chung et al. [28] reported that among beef
and pork samples cooked by grilling and roasting methods, the highest BaP and ZPAH4 content was observed in the grilled samples. In addition, the researchers stated that this may be related to the pyrolysis of meat fat dripping onto the charcoal during grilling. In another study examining the effects of different cooking processes (smoking, grilling and boiling) on PAH formation in different meat products, the highest BaP content was found in the smoked samples while the lowest BaP content was detected in boiled samples [29]. As a result of the studies examining the effect of different cooking methods on the level of PAH formed in meat and meat products, it was reported that meat samples cooked by grilling, smoking and roasting methods carry a high health risk due to their high PAH content [28].
Another factor affecting the PAH level formed during the cooking of meat; is the practice of cooking by direct or indirect method. While the direct method is based on the principle of direct contact of meat with a thermal agent, in the indirect method, a thermal agent does not affect the cooked meat through direct contact. Many studies confirm that direct contact with heat source increases PAH formation and that food retains PAH compounds through adsorption and absorption [32]. In [33], the ZPAH16 content
Figure 1. Factors affecting the formation of PAH compounds
of beef cooked with the electric oven grill, which is an indirect cooking technique, was determined as 2.01 ^g/kg, while this value was reported to be 17.88 ^g/kg in the samples cooked with the charcoal grill method, a direct cooking technique. El-Badry [34] found that direct contact with the gas flame promoted the formation of PAH in the chicken. The author [34] also reported that cooking chicken meat with the direct gas grill cooking technique should be avoided. Wretling et al. [35] stated that the BaP and 2PAH15 content of the various meat samples smoked by the traditional "sauna" method, in which the samples are exposed directly to the hot smoke from a burning fire, were above the legal limits. Akpambang et al. [36] reported that the use of the indirect smoking technique instead of the direct smoking method is quite effective in reducing PAH formation in smoked meat products.
Free radicals formed when high temperatures are applied to foods undergo recombination to form light PAHs. Heavy PAHs that migrate to the hydrophobic portions of the food following this formation eventually attach to the fat-rich food portions [32]. In this context, the level of PAH formation and accumulation in meat may vary depending on the lipid level of meat. Wegrzyn et al. [37] reported that the fat content is an important parameter that can affect the safety of meat in terms of PAH compounds. Particularly, in meat and meat products where grill and barbecue cooking methods are applied, PAH compounds can be formed that are carried back to the meat surface as a result of the pyrolysis of meat fat or dripping into the flame [13]. The fat content of meat is an important factor influencing the level of PAH formed when this type of cooking method is used. In a study examining the effect of fat content on PAH formation in various grilled meat samples, it was determined that the BaP content of lamb steak, which had the highest fat content, was higher than that of beef steak, pork chop and ham. It has been reported that this result may be related to the formation of more lipid oxidation and degradation products in lamb steak with the high fat content [38]. Pohlmann et al. [39] conducted a study to determine an effect of the fat content on PAH formation in smoked frankfurter sausages and found that the 2PAH4 level of sausages with different fat contents (10, 20, 30 and 39%) increased with an increase in the fat content. They also reported that PAH formation in smoked frankfurter sausages could be reduced by reducing the fat content in the sausage formulation. In addition to an amount of fat, a type of fat can also affect the formation of PAH. As a matter of fact, Chen and Chen [40] examined the PAH level of smoke formed as a result of heat treatment of soybean oil, canola and sunflower oils and determined that the highest total PAH amount was in soybean oil. Researchers reported that this result was related to the higher levels of linolenic acid in soybean oil compared to canola and sunflower oils. Similarly, in a study examining the PAH level of meatballs cooked in barbecue using different types of fat (meat fat, sheep tail fat and a mixture of meat fat and tail fat), it was
determined that the highest total PAH8 level belonged to the meatballs formulated with tail fat, which had the highest linolenic acid content [3].
The cooking process, including temperature and time, and a distance between meat and a heat source are the factors affecting the PAH formation. Literature data indicate that the level of PAH formed in meat increases in parallel with an increase in cooking temperature and time. According to Kao et al. [41] reported that high temperature and long cooking time cause more fat loss from the meat surface, which may cause a heat source to produce more PAH. In a study, in which an effect of cooking time on the PAH content of grilled pork was determined, the BaP contents of the samples cooked for 2, 3 and 4 minutes were found to be 2.4 ^g/kg, 4.5 ^g/kg and 10.2 ^g/kg, respectively. In addition, it has been reported that the BaP level formed as a result of cooking for 4 minutes has reached the legal limit specified by the European Commission [42]. Oz and Yuzer [30] found that the total PAH8 content of well-done and very well-done beef samples in wire barbecue was 0.8 and 0.9 mg/kg, respectively, while they could not detect any of the individual PAH compounds that make up PAH8 in rare and medium cooked beef. In another study examining the PAH level of a traditional Malaysian beef product, cooking was done at different temperatures (150 °C, 200 °C, 250 °C, 300 °C and 350 °C). As a result of the research, it was reported that the lowest 2PAH15 level was detected in the samples grilled at 150 °C and an increase in the 2PAH15 level was observed as the temperature increased [43]. Sz-terk [44] reported that PAH formation increased as a result of high temperature application due to the pyrolysis of nitrogen-containing organic compounds such as amino acids and protein. In a study examining an effect of smoking time on PAH formation in meat products, it was found that both BaP and 2PAH4 amounts were higher in meat samples with high smoking time [45]. On the other hand, studies on a distance between food and a heat source, which is another factor affecting PAH formation, show that there is a negative correlation between distance and PAH formation in general. Roseiro et al. [46] examined an effect of smoking distance on PAH formation in sausages and reported that as the distance decreased PAH penetrated into the central point of the sausages. In [11] Rose et al. determined that the 2PAH4 content of beef burgers cooked at a distance of 9 cm from the heat source was 75% of the 2PAH4 content of the samples cooked at a distance of 4 cm from the heat source. This relationship between distance and PAH formation is probably related to an increase in the rate of PAH formation and penetration into the sample that comes into contact with hot and intense heat more quickly in short distance.
PAH formation occurs due to the acetylene addition mechanism (HACA) with the release of hydrogen during the combustion of the fuel used in the thermal process. On the other hand, the level of PAH formed may vary depending on a type of fuel used [10]. In the report published
by the Codex Alimentarius Commission in 2009, it was recommended not to use resinous or chemically treated woods, waste or diesel oils as fuel in cooking process [47]. In [48] Viegas et al. examined an effect of fuel type on the PAH level of grilled salmon and reported that the samples grilled with coconut shell charcoal produced less PAH than the samples grilled with usual wood charcoal. The authors stated that this result is related to the ability of coconut charcoal to absorb dripping oil without creating smoke, since it is flameless and smokeless [48]. Oz [12] found that amounts of 2PAH8 were higher in fish samples barbecued with charcoal briquette compared to those barbecued with wood charcoal, and suggested the use of wood charcoal in barbecuing. In another study examining the PAH levels of chicken meat cooked using charcoal and electric grill, it was determined that the average 2PAH16 level of chicken meat cooked with charcoal and electric grill was 1.6 |g/kg, and 0.038 |g/kg, respectively [49]. Similarly, it was determined that the BaP content of doner kebabs cooked on charcoal and gas grills was 24.2 |g/kg and 5.7 |g/kg, respectively, and gas grilling caused less BaP formation [50]. Oz [2] reported that a type of smoke flavoring wood chips affected the level of PAH formation in barbecued salmon fillets, and bourbon-soaked oak, cherry and hickory wood chips were the wood chips types that could reduce the content of PAHs in barbecued salmon fillets. Stumpe-Viksna et al. [51] reported that a type of sawdust is a critical parameter to be controlled in the smoking process, and that softwood shavings cause higher PAH formation than hardwood shavings, possibly due to the high resin content they contain.
Pre-cooking is one of the strategies applied to reduce PAH formation in cooked meat. Ohmic heating is a widely used technique in recent years due to its advantages such as short processing time, high efficiency and preservation of the nutritional value compared to conventional heating methods [52]. Sengun et al. studied an effect of ohmic preheating on the PAH level of half-cooked meatballs and found that the PAH levels of the meatballs were within acceptable limits, and therefore the ohmic cooking method was safe in terms of PAH formation [53]. In [54] Kend-irci et al. determined an effect of ohmic preheating before infrared cooking on PAH formation in beef patties. They reported that the BaP and 2PAH4 contents formed as a result of the combination of preheating and infrared cooking did not exceed the legal limits [54]. Farhadian et al. [55] investigated an effect of preheating processes (steam and microwave) on PAH levels in grilled chicken and beef. They established that preheating processes applied to the samples strongly affected PAH levels and BaP could not be detected in pretreated samples. The authors stated that this situation may be related to a decrease in the pyrolysis rate as a result of preheating and less penetration of the smoke components into the meat surface and suggested to expand the use of preheating processes in homes and restaurants in order to reduce PAH exposure [55].
Marinating is a technique commonly used to improve the sensory properties of meat products such as texture, color and flavor. Studies on the effect of the marination on the formation of PAH in meat reveal that the effect varies depending on a type of marinade used. Farhadian et al. [56] reported that the PAH content in grilled beef marinated with basic marinades varied between 45.19-56.09 |g/kg, while this value varied between 74.0-80.6 |g/kg in the un-marinated control samples. On the other hand, researchers mentioned that adding 40 mL of oil into basic marination increased the PAH content of grilled beef meat (98.9109 |g/kg). Similarly, it has been shown in some studies that oil and fatty components are major precursors of PAHs and that cooking oils can be contaminated with PAHs during various preparation processes [57,58]. In a study examining the level of PAH in grilled chicken, the 2PAH16 amount of unmarinated, palm oil-marinated and sunflower oil-marinated samples was determined as 190.1|g/kg, 457.6 |g/kg and 376.6 |g/kg, respectively. In addition, it has been reported that an increase in the PAH content observed as a result of marinating with oil is related to the fact that oils are the main precursors of PAH components [59]. In [31] Büyükkurt et al. used sage and thyme extracts prepared at 0.5-2.0 °Brix concentration as a marination agent and reported that these marinades showed a reducing effect on PAH formation in barbecued beef. Viegas et al. [60] determined that marinating with different types of beer reduced the amount of 2PAH8 formed in grilled pork by 13-53%, depending on a type of beer used. They also reported that the greatest decrease in the PAH content was observed in dark beer marinated samples, which had the highest antiradical activity. Janoszka [61] found that the use of onion (30/100 g meat) caused a 60% reduction in the total PAH content of pan-fired meat, while the use of garlic (15/100 g meat) resulted in a 54% reduction. It has been declared that the PAH-lowering effect of onion and garlic may be caused by components with sulfhydryl groups, and polyphenols responsible for the antioxidant activity [61,62]. In a study examining an effect of using a spice mixture containing cumin, coriander, black pepper, rosemary and garlic on the formation of carcinogenic PAHs in chicken meat, it was determined that the spice mixture caused a significant decrease in the level of carcinogenic PAHs. In addition, it has been suggested to use the specified mixture before cooking chicken meat in order to reduce the level of PAHs [34].
Conclusion
PAHs are a large group of environmental pollutants with mutagenic and/or carcinogenic properties. Foodstuffs are the main sources of PAH exposure. Among food groups, meat and meat products being rich in protein and fat contribute significantly to PAH exposure due to the frequent use of thermal processes and increased risk depending on consumption habits. Many factors such as cooking method, thermal process duration, fuel/wood type, pre-cooking applications, marination, additives and
fat content of meat affect the level of PAH in meat and meat moderate and indirect heat processes in cooking, to use products. In this context, in order to reduce the amount non-smoke fuel types, to add antioxidants and to reduce of PAH formed in meat, it can be recommended to apply the fat content of meat.
REFERENCES
1. Plaza-Bolanos, P., Frenich, A. G., Vidal, J. L. M. (2010). Polycyclic aromatic hydrocarbons in food and beverages. Analytical methods and trends. Journal of Chromatography A, 1217(41), 6303-6326. https://doi.org/10.1016/j.chroma.2010.07.079
2. Oz, E. (2020). Effects of smoke flavoring using different wood chips and barbecuing on the formation of polycyclic aromatic hydrocarbons and heterocyclic aromatic amines in salmon fillets. PLoS One, 15(1), Article e0227508. https://doi.org/10.1371/ journal.pone.0227508
3. Oz, E. (2021). The presence of polycyclic aromatic hydrocarbons and heterocyclic aromatic amines in barbecued meatballs formulated with different animal fats. Food Chemistry, 352, Article 129378. https://doi.org/10.1016/j.foodchem.2021.129378
4. Purcaro, G., Moret, S., Conte, L. S. (2013). Overview on polycy-clic aromatic hydrocarbons: Occurrence, legislation and innovative determination in foods. Talanta, 105, 292-305. https://doi. org/10.1016/j.talanta.2012.10.041
5. Bogdanovic, T., Pleadin, J., Petricevic, S., Listes, E., Sokolic, D., Markovic, K. et al. (2019). The occurrence of polycyclic aromatic hydrocarbons in fish and meat products of Croatia and dietary exposure. Journal of Food Composition and Analysis, 75, 49-60. https://doi.org/10.1016/j.jfca.2018.09.017
6. Storelli, M. M., Stuffier, R. G., Marcotrigiano, G. O. (2003). Poly-cyclic aromatic hydrocarbons, polychlorinated biphenyls, chlorinated pesticides (DDTs), hexachlorocyclohexane, and hexachloroben-zene residues in smoked seafood. Journal of Food Protection, 66(6), 1095-1099. https://doi.org/10.4315/0362-028X-66.6.1095
7. Li, Y., Wang, C., Zou, X., Feng, Z., Yao, Y., Wang, T. et al. (2019). Occurrence of polycyclic aromatic hydrocarbons (PAHs) in coral reef fish from the South China Sea. Marine Pollution Bulletin, 139, 339-345. https://doi.org/10.1016/j.marpolbul.2019.01.001
8. Singh, L., Agarwal, T., Simal-Gandara, J. (2020). PAHs, diet and cancer prevention: Cooking process driven-strategies. Trends in Food Science and Technology, 99, 487-506. https://doi. org/10.1016/j.tifs.2020.03.030
9. Wang, L., Li, C., Jiao, B., Li, Q., Su, H., Wang, J. et al. (2018). Halogenated and parent polycyclic aromatic hydrocarbons in vegetables: levels, dietary intakes, and health risk assessments. Science of the Total Environment, 616-617, 288-295. https://doi. org/10.1016/j.scitotenv.2017.10.336
10. Sun, Y., Wu, S., Gong, G. (2019). Trends of research on poly-cyclic aromatic hydrocarbons in food: A 20-year perspective from 1997 to 2017. Trends in Food Science and Technology, 83, 86-98. https://doi.org/10.1016/j.tifs.2018.11.015
11. Rose, M., Holland, J., Dowding, A., Petch, S. R. G., White, S., Fernandes, A. et al. (2015). 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, 78, 1-9. https://doi.org/10.1016/j. fct.2014.12.018
12. Oz, E. (2021). The impact of fat content and charcoal types on quality and the development of carcinogenic polycyclic aromatic hydrocarbons and heterocyclic aromatic amines formation of barbecued fish. International Journal of Food Science and Technology, 56(2), 954-964. https://doi.org/10.1111/ijfs.14748
13. Zelinkova, Z., Wenzl, T. (2015). The occurrence of 16 EPA PAHs in food — A review. Polycyclic Aromatic Compounds, 35(2-4), 248284. https://doi.org/10.1080/10406638.2014.918550
14. Duedahl-Olesen, L., Ionas, A. C. (2022). Formation and mitigation of PAHs in barbecued meat — a review. Critical Reviews in Food Science and Nutrition, 62(13), 3553-3568. https://doi.org /10.1080/10408398.2020.1867056
15. Onopiuk, A., Kolodziejczak, K., Szpicer, A., Wojtasik-Kalin-owska, I., Wierzbicka, A., Poltorak, A. (2021). Analysis of factors that influence the PAH profile and amount in meat products subjected to thermal processing. Trends in Food Science and Technology, 115, 366-379. https://doi.org/10.1016/j.tifs.2021.06.043
16. Rengarajan, T., Rajendran, P., Nandakumar, N., Lokeshkumar, B., Rajendran, P., Nishigaki, I. (2015). Exposure to polycyclic aromatic hydrocarbons with special focus on cancer. Asian Pacific Journal of Tropical Biomedicine, 5(3), 182-189. https://doi. org/10.1016/S2221-1691(15)30003-4
17. Cross, A. J., Freedman, N. D., Ren, J., Ward, M. H., Hollenbeck, A. R., Schatzkin, A. et al. (2011). Meat consumption and risk of esophageal and gastric cancer in a large prospective study. The American Journal of Gastroenterology, 106(3), 432-442. https://doi.org/10.1038/ajg.2010.41B
18. Zhu, Z., Xu, Y., Huang, T., Yu, Y., Bassey, A. P., Huang, M. (2022). The contamination, formation, determination and control of polycyclic aromatic hydrocarbons in meat products. Food Control, 141, Article 109194. https://doi.org/10.1016/j.food-cont.2022.109194
19. IARC (International Agency for Research on Cancer). (2010). Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, France, 2010.
20. EPA (Environmental Protection Agency). (2008). Polycyclic aromatic hydrocarbons (PAHs) — EPA fact sheet. Washington (DC): National Center for Environmental Assessment, Office of Research and Development, 2008.
21. Abdel-Shafy, H. I., Mansour, M. S. (2016). A review on polycy-clic aromatic hydrocarbons: Source, environmental impact, effect on human health and remediation. Egyptian Journal of Petroleum, 2B(1), 107-123. https://doi.org/10.1016/j.ejpe.201B.03.011
22. Daniel, C. R., Schwartz, K. L., Colt, J. S., Dong, L. M., Ruter-busch, J. J., Purdue, M. P. et al. (2011). Meat-cooking mutagens and risk of renal cell carcinoma. British Journal of Cancer, 10B(7), 1096-1104. https://doi.org/10.1038/bjc.2011.343
23. Alomirah, H., Al-Zenki, S., Al-Hooti, S., Zaghloul, S., Sawaya, W., Ahmed, N. et al. (2011). Concentrations and dietary exposure to polycyclic aromatic hydrocarbons (PAHs) from grilled and smoked foods. Food Control, 22(12), 2028-203B. https://doi. org/10.1016/j.foodcont.2011.0B.024
24. Ledesma, E., Rendueles, M., Díaz, M. J. F. C. (2016). Contamination of meat products during smoking by polycyclic aromatic hydrocarbons: Processes and prevention. Food Control, 60, 6487. https://doi.org/10.1016/j.foodcont.201B.07.016
2B. EFSA. (2008). Scientific opinion of the panel on contaminants in the food chain on a request from the European Commission on Polycyclic Aromatic Hydrocarbons in Food. The EFSA Journal, 724, 1-114.
26. Commission Regulation (EU). (2011). No: 83B/2011 of 19 August 2011 amending Regulation (EC) No: 1881/2006 as regards maximum levels for polycyclic aromatic hydrocarbons in foodstuff.
27. Perelló, G., Martí-Cid, R., Castell, V., Llobet, J. M., Domingo, J. L. (2009). Concentrations of polybrominated diphenyl ethers, hexachlorobenzene and polycyclic aromatic hydrocarbons in various foodstuffs before and after cooking. Food and Chemical Toxicology, 47(4), 709-71B. https://doi.org/10.1016/j. fct.2008.12.030
28. Chung, S. Y., Yettella, R. R., Kim, J. S., Kwon, K., Kim, M. C., Min, D. B. (2011). Effects of grilling and roasting on the levels of polycyclic aromatic hydrocarbons in beef and pork. Food Chemistry, 129(4), 1420-1426. https://doi.org/10.1016/j.food-chem.2011.0B.092
29. Olatunji, O. S., Fatoki, O. S., Ximba, B. J., Opeolu, B. O. (2014). Polycyclic aromatic hydrocarbons (PAHs) in edible oil: temperature effect on recovery from base hydrolysis product and health risk factor. Food and Public Health, 4(2), 23-30. https://doi. org/10.B923/j.fph.20140402.02
30. Oz, F., Yuzer, M. O. (2016). 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, 203, B9-66. https://doi. org/10.1016/j.foodchem.2016.02.041
31. Büyükkurt, O. K., Dinçer, E. A., Çam, I. B., Candal, C., Erbaç, M. (2017). The influence of cooking methods and some marinades on polycyclic aromatic hydrocarbon formation in beef meat. Poly-cyclic Aromatic Compounds, 40(2), 19B-20B. https://doi.org/10 .1080/10406638.2017.1392328
32. Singh, L., Varshney, J. G., Agarwal, T. (2016). Polycyclic aromatic hydrocarbons' formation and occurrence in processed food. Food Chemistry, 199, 768-781. https://doi.org/10.1016/j. foodchem.201B.12.074
33. Onyango, A. A., Lalah, J. O., Wandiga, S. O. (2012). The effect of local cooking methods on polycyclic aromatic hydrocarbons (PAHs) contents in beef, goat meat, and pork as potential sources of human exposure in Kisumu city, Kenya. Polycyclic Aromatic Compounds, 32(5), 656-668. https://doi.org/10.1080/10 406638.2012.725195
34. El-Badry, N. (2010). Effect of household cooking methods and some food additives on polycyclic aromatic hydrocarbons (PAHs) formation in chicken meat. World Applied Sciences Journal, 9(9), 963-974.
35. Wretling, S., Eriksson, A., Eskhult, G. A., Larsson, B. (2010). Polycyclic aromatic hydrocarbons (PAHs) in Swedish smoked meat and fish. Journal of Food Composition and Analysis, 23(3), 264-272. https://doi.org/10.1016Zj.jfca.2009.10.003
36. Akpambang, V. O. E., Purcaro, G., Lajide, L., Amoo, I. A., Conte, L. S., Moret, S. (2009). Determination of polycyclic aromatic hydrocarbons (PAHs) in commonly consumed Nigerian smoked/grilled fish and meat. Food Additives and Contaminants: Part A, 26(7), 1096-1103. https://doi.org/10.1080/02652030902855406
37. Wegrzyn, E., Grzeskiewicz, S., Poplawska, W., Glod, B. K. (2006). Modified analytical method for polycyclic aromatic hydrocarbons, using sec for sample preparation and RP-HPLC with fluorescence detection. Application to different food samples. Acta Chromatographica, 17, 233.
38. Kao, T. H., Chen, S., Huang, C. W., Chen, C. J., Chen, B. H. (2014). Occurrence and exposure to polycyclic aromatic hydrocarbons in kindling-free-charcoal grilled meat products in Taiwan. Food and Chemical Toxicology, 71, 149-158. https://doi. org/10.1016/j.fct.2014.05.033
39. Pohlmann, M., Hitzel, A., Schwagele, F., Speer, K., Jira, W. (2013). Polycyclic aromatic hydrocarbons (PAH) and phenolic substances in smoked Frankfurter-type sausages depending on type of casing and fat content. Food Control, 31(1), 136-144. https://doi.org/10.1016/j.foodcont.2012.09.030
40. Chen, B. H., Chen, Y. C. (2001). Formation of polycyclic aromatic hydrocarbons in the smoke from heated model lipids and food lipids. Journal of Agricultural and Food Chemistry, 49(11), 5238-5243. https://doi.org/10.1021/jf0106906
41. Kao, T. H., Chen, S., Chen, C. J., Huang, C. W., Chen, B. H. (2012). Evaluation of analysis of polycyclic aromatic hydrocarbons by the QuEChERS method and gas chromatography-mass spectrometry and their formation in poultry meat as affected by marinating and frying. Journal of Agricultural and Food Chemistry, 60(6), 1380-1389. https://doi.org/10.1021/jf204650u
42. Pan, H., Cao, Y. (2010). Optimization of pretreatment procedures for analysis of polycyclic aromatic hydrocarbons in charcoal-grilled pork. Analytical Letters, 43(1), 97-109. https://doi. org/10.1080/00032710903276497
43. Ahmad Kamal, N. H., Selamat, J., Sanny, M. (2018). Simultaneous formation of polycyclic aromatic hydrocarbons (PAHs) and heterocyclic aromatic amines (HCAs) in gas-grilled beef satay at different temperatures. Food Additives and Contaminants: Part A, 35(5), 848-869. https://doi.org/10.1080/19440049.2018.1425553
44. Szterk, A. (2015). Acridine derivatives (PANHs, azaarenes) in raw, fried or grilled pork from different origins, and PANH formation during pork thermal processing. Journal of Food Composition and Analysis, 43, 18-24. https://doi.org/10.1016/jjfca.2015.04.011
45. Hokkanen, M., Luhtasela, U., Kostamo, P., Ritvanen, T., Pel-tonen, K., Jestoi, M. (2018). Critical effects of smoking parameters on the levels of polycyclic aromatic hydrocarbons in traditionally smoked fish and meat products in Finland. Journal of Chemistry, 2018, Article 2160958. https://doi.org/10.1155/2018/2160958
46. Roseiro, L. C., Gomes, A., Santos, C. (2011). Influence of processing in the prevalence of polycyclic aromatic hydrocarbons in a Portuguese traditional meat product. Food and Chemical Toxicology, 49(6), 1340-1345. https://doi.org/10.1016/j.fct.2011.03.017
47. CAC/RCP 68 (2009). Codex alimentarius commission (CAC). Code of practice for the reduction of contamination of food with
polycyclic aromatic hydrocarbons (PAH) from smoking and direct drying processes.
48. Viegas, O., Novo, P., Pinto, E., Pinho, O., Ferreira, I. M. P. L. V. O. (2012). 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, 50(6), 2128-2134. https://doi.org/10.1016/j.fct.2012.03.051
49. Hamzawy, A. H., Khorshid, M., Elmarsafy, A. M., Souaya, E. R. (2016). Estimated daily intake and health risk of polycyclic aromatic hydrocarbon by consumption of grilled meat and chicken in Egypt. International Journal of Current Microbiology and Applied Sciences, 5(2), 435-448. http://doi.org/10.20546/ijcmas.2016.502.049
50. Terzi, G., Celik, T. H., Nisbet, C. (2008). Determination of benzo[a] pyrene in Turkish doner kebab samples cooked with charcoal or gas fire. Irish Journal of Agricultural and Food Research, 47(2), 187-193.
51. Stumpe-Viksna, I., Bartkevics, V., Kukare, A., Morozovs, A. (2008). Polycyclic aromatic hydrocarbons in meat smoked with different types of wood. Food Chemistry, 110(3), 794-797. http://doi.org/10.1016/j.foodchem.2008.03.004
52. Yildiz-Turp, G., Sengun, I. Y., Kendirci, P., Icier, F. (2013). Effect of ohmic treatment on quality characteristic of meat: A review. Meat Science, 93(3), 441-448. http://doi.org/10.1016/j. meatsci.2012.10.013
53. Sengun, I. Y., Yildiz-Turp, G., Icier, F., Kendirci, P., Kor, G. (2014). Effects of ohmic heating for pre-cooking of meatballs on some quality and safety attributes. LWT-Food Science and Technology, 55(1), 232-239. http://doi.org/10.1016/j.lwt.2013.08.005
54. Kendirci, P., Icier, F., Kor, G., Onogur, T. A. (2014). Influence of infrared final cooking on polycyclic aromatic hydrocarbon formation in ohmically pre-cooked beef meatballs. Meat Science, 97(2), 123-129. http://doi.org/10.1016/j.meatsci.2014.01.020
55. Farhadian, A., Jinap, S., Hanifah, H. N., Zaidul, I. S. (2011). Effects of meat preheating and wrapping on the levels of polycyclic aromatic hydrocarbons in charcoal-grilled meat. Food Chemistry, 124(1), 141-146. http://doi.org/10.1016/j.foodchem.2010.05.116
56. Farhadian, A., Jinap, S., Faridah, A., Zaidul, I. S. M. (2012). Effects of marinating on the formation of polycyclic aromatic hydrocarbons (benzo[a]pyrene, benzo[b]fluoranthene and fluoranthene) in grilled beef meat. Food Control, 28(2), 420-425. http://doi. org/10.1016/j.foodcont.2012.04.034
57. McGrath, T. E., Wooten, J. B., Chan, W. G., Hajaligol, M. R. (2007). Formation of polycyclic aromatic hydrocarbons from tobacco: the link between low temperature residual solid (char) and PAH formation. Food and Chemical Toxicology, 45(6), 10391050. http://doi.org/10.1016/j.fct.2006.12.010
58. Rojo Camargo, M. C., Antoniolli, P. R., Vicente, E., Tfouni, S. A. V. (2011). Polycyclic aromatic hydrocarbons in Brazilian commercial soybean oils and dietary exposure. Food Additives and Contaminants: Part B, 4(2), 152-159. https://doi.org/10.1080/193 93210.2011.585244
59. Wongmaneepratip, W., Vangnai, K. (2017). Effects of oil types and pH on carcinogenic polycyclic aromatic hydrocarbons (PAHs) in grilled chicken. Food Control, 79, 119-125. https://doi. org/10.1016/j.foodcont.2017.03.029
60. Viegas, O., Yebra-Pimentel, I., Martinez-Carballo, E., Simal-Gandara, J., Ferreira, I. M. P. L. V. O. (2014). Effect of beer marinades on formation of polycyclic aromatic hydrocarbons in charcoal-grilled pork. Journal of Agricultural and Food Chemistry, 62(12), 2638-2643. https://doi.org/10.1021/jf404966w
61. Janoszka, B. (2011). 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, 126(3), 1344-1353. https://doi.org/10.1016/j.food-chem.2010.11.097
62. Bianchini, F., Vainio, H. (2001). Allium vegetables and or-ganosulfur compounds: do they help prevent cancer? Environmental Health Perspectives, 109(9), 893-902. https://doi. org/10.1289/ehp.01109893
AUTHOR INFORMATION
Emel Oz, PhD, Associate Professor, Department of Food Engineering, Faculty of Agriculture, Ataturk University. 25240, Erzurum, Turkey. Tel.: +904-42-231-16-25, E-mail: emel.oz@atauni.edu.tr ORCID: https://orcid.org/0000-0003-3766-2713
Completely prepared the manuscript and is responsible for plagiarism.
The author declare no conflict of interest.
