Browse > Article
http://dx.doi.org/10.5187/jast.2022.e86

Study on the reduction of heterocyclic amines by marinated natural materials in pork belly  

Hea Jin, Kang (Department of Animal Science and Technology, Chung-Ang University)
Seung Yun, Lee (Department of Animal Science and Technology, Chung-Ang University)
Da Young, Lee (Department of Animal Science and Technology, Chung-Ang University)
Ji Hyeop, Kang (Department of Animal Science and Technology, Chung-Ang University)
Jae Hyeon, Kim (Department of Animal Science and Technology, Chung-Ang University)
Hyun Woo, Kim (Department of Animal Science and Technology, Chung-Ang University)
Jae Won, Jeong (Department of Animal Science and Technology, Chung-Ang University)
Dong Hoon, Oh (Department of Animal Science and Technology, Chung-Ang University)
Sun Jin, Hur (Department of Animal Science and Technology, Chung-Ang University)
Publication Information
Journal of Animal Science and Technology / v.64, no.6, 2022 , pp. 1245-1258 More about this Journal
Abstract
This study was conducted to determine the effect of natural ingredient seasoning on the reduction of heterocyclic amine (HCA) production that may occur when pork belly is cooked at a very high temperature for a long time. Pork belly seasoned with natural ingredients, such as natural spices, blackcurrant, and gochujang, was cooked using the most common cooking methods, such as boiling, pan fry, and barbecue. HCAs in pork belly were extracted through solid-phase extraction and analyzed via high-performance liquid chromatography. For short-term toxicity, a mouse model was used to analyze weight, feed intake, organ weight, and length; hematology and serology analysis were also performed. Results revealed that HCAs formed only when heating was performed at a very high temperature for a long time, not under general cooking conditions. Although the toxicity levels were not dangerous, the method showing the relatively highest toxicity among various cooking methods was barbecue, and the natural material with the highest toxicity reduction effect was blackcurrant. Furthermore, seasoning pork belly with natural materials containing a large amount of antioxidants, such as vitamin C, can reduce the production of toxic substances, such as HCAs, even if pork belly is heated to high temperatures.
Keywords
Pork belly; Heterocyclic amines; Natural materials; Blackcurrant; Antioxidants;
Citations & Related Records
Times Cited By KSCI : 10  (Citation Analysis)
연도 인용수 순위
1 Nour V, Trandafir I, Ionica ME. Ascorbic acid, anthocyanins, organic acids and mineral content of some black and red currant cultivars. Fruits. 2011;66:353-62. https://doi.org/10.1051/fruits/2011049   DOI
2 Moyer RA, Hummer KE, Finn CE, Frei B, Wrolstad RE. Anthocyanins, phenolics, and antioxidant capacity in diverse small fruits: Vaccinium, Rubus, and Ribes. J Agric Food Chem. 2002;50:519-25. https://doi.org/10.1021/jf011062r   DOI
3 Paredes-Lopez O, Cervantes-Ceja ML, Vigna-Perez M, Hernandez-Perez T. Berries: improving human health and healthy aging, and promoting quality life-a review. Plant Foods Hum Nutr. 2010;65:299-308. https://doi.org/10.1007/s11130-010-0177-1   DOI
4 Kim SJ, Jung KO. In vitro anticancer effect of kochujang (Korean red pepper soybean paste) and its ingredients in AGS human gastric cancer cells. J Korean Assoc Cancer Prev. 2004;9:42-8.
5 Borges G, Degeneve A, Mullen W, Crozier A. Identification of flavonoid and phenolic antioxidants in black currants, blueberries, raspberries, red currants, and cranberries. J Agric Food Chem. 2010;58:3901-9. https://doi.org/10.1021/jf902263n   DOI
6 Platt KL, Edenharder R, Aderhold S, Muckel E, Glatt H. Fruits and vegetables protect against the genotoxicity of heterocyclic aromatic amines activated by human xenobiotic-metabolizing enzymes expressed in immortal mammalian cells. Mutat Res Genet Toxicol Environ Mutagen. 2010;703:90-8. https://doi.org/10.1016/j.mrgentox.2010.08.007   DOI
7 Kim S, Oh J, Jang CH, Kim JS. Improvement of cognitive function by Gochujang supplemented with tomato paste in a mouse model. Food Sci Biotechnol. 2019;28:1225-33. https://doi.org/10.1007/s10068-019-00565-0   DOI
8 Kim HJ, Cho J, Kim D, Park TS, Jin SK, Hur SJ, et al. Effects of Gochujang (Korean red pepper paste) marinade on polycyclic aromatic hydrocarbon formation in charcoal-grilled pork belly. Food Sci Anim Resour. 2021;41:481-96. https://doi.org/10.5851/kosfa.2021.e12   DOI
9 Yang HJ, Lee YS, Choi IS. Comparison of physicochemical properties and antioxidant activities of fermented soybean-based red pepper paste, Gochujang, prepared with five different red pepper (Capsicum annuum L.) varieties. J Food Sci Technol. 2018;55:792-801. https://doi.org/10.1007/s13197-017-2992-y   DOI
10 Chung JY, Kim CS. Antioxidant activities of domestic garlic (Allium sativum L.) stems from different areas. J Korean Soc Food Sci Nutr. 2008;37:972-8. https://doi.org/10.3746/jkfn.2008.37.8.972   DOI
11 Lee HR, Lee JH, Park CS, Ra KR, Ha JS, Cha MH, et al. Physicochemical properties and antioxidant capacities of different parts of ginger (Zingiber officinale Roscoe). J Korean Soc Food Sci Nutr. 2014;43:1369-79. https://doi.org/10.3746/jkfn.2014.43.9.1369   DOI
12 Ohta T, Watanabe K, Moriya M, Shirasu Y, Kada T. Antimutagenic effects of cinnamaldehyde on chemical mutagenesis in Escherichia coli. Mutat Res. 1983;107:219-27. https://doi.org/10.1016/0027-5107(83)90164-1   DOI
13 Lee AY, Kim HS, Choi G, Chun JM, Moon BC, Kim HK. Comparison of major compounds in Illicii Veri Fructus by extraction solvents. Korea J Herbol. 2013;28:47-51. https://doi.org/10.6116/kjh.2013.28.6.47   DOI
14 Park CH, Kim JH, Choi SH, Shin YS, Lee SW, Cho EJ. Protective effects of Glycyrrhiza uralensis Radix extract and its active compounds on H2O2-induced apoptosis of C6 glial cells. Korean J Med Crop Sci. 2017;25:315-21. https://doi.org/10.7783/KJMCS.2017.25.5.315   DOI
15 Pearson AM, Gillett TA. Least cost formulation and preblending of sausage. In: Pearson AM, Gillett TA, editors. Processed meats. Boston, MA: Springer; 1996. p. 180-209.
16 Barido FH, Utama DT, Kim YJ, Lee SK. Fatty acid profiles and flavour-related compounds of retorted Korean ginseng chicken soup (Samgyetang) affected by pre-treated black garlic extract. Anim Biosci. 2022;35:1080-90. https://doi.org/10.5713/ab.21.0575   DOI
17 Yanishlieva NV, Marinova E, Pokorny J. Natural antioxidants from herbs and spices. Eur J Lipid Sci Technol. 2006;108:776-93. https://doi.org/10.1002/ejlt.200600127   DOI
18 Lee HJ, Yoon D, Lee N, Lee C. Effect of aged and fermented garlic extracts as natural antioxidants on lipid oxidation in pork patties. Food Sci Anim Resour. 2019;39:610-22. https://doi.org/10.5851/kosfa.2019.e51   DOI
19 Gross GA, Gruter A. Quantitation of mutagegnic/carcinogenic heterocyclic aromatic amines in food products. J Chromatogr A. 1992;592:271-8. https://doi.org/10.1016/0021-9673(92)85095-B   DOI
20 Zhao K, Murray S, Davies DS, Boobis AR, Gooderham NJ. Metabolism of the food derived mutagen and carcinogen 2-amino-1-methyl-6-phnylimidazo(4,5-b)pyridine (PhIP) by human liver microsomes. Carcinogenesis. 1994;15:1285-8. https://doi.org/10.1093/carcin/15.6.1285   DOI
21 van Boekel MAJS. Formation of flavour compounds in the Maillard reaction. Biotechnol Adv. 2006;24:230-3. https://doi.org/10.1016/j.biotechadv.2005.11.004   DOI
22 Kang HJ, Lee SY, Lee DY, Kang JH, Kim JH, Kim HW, et al. Main mechanisms for carcinogenic heterocyclic amine reduction in cooked meat by natural materials. Meat Sci. 2022;183:108663. https://doi.org/10.1016/j.meatsci.2021.108663   DOI
23 Murkovic M. Formation of heterocyclic aromatic amines in model systems. J Chromatogr B. 2004;802:3-10. https://doi.org/10.1016/j.jchromb.2003.09.026   DOI
24 Zhang H, Yang J, Zhao Y. High intensity ultrasound assisted heating to improve solubility, antioxidant and antibacterial properties of chitosan-fructose Maillard reaction products. LWT - Food Sci Technol. 2015;60:253-62. https://doi.org/10.1016/j.lwt.2014.07.050   DOI
25 O'Brien J, Morrissey PA, Ames JM. Nutritional and toxicological aspects of the Maillard browning reaction in foods. Crit Rev Food Sci Nutr. 1989;28:211-48. https://doi.org/10.1080/10408398909527499   DOI
26 Ismarti I, Triyana K, Fadzillah NA, Nordin NFH. The significance of Maillard reaction for species-specific detection gelatine in food industry. J Phys Conf Ser. 2021;1731:012018. https://doi.org/10.1088/1742-6596/1731/1/012018   DOI
27 Gibis M, Loeffler M. Effect of creatine and glucose on formation of heterocyclic amines in grilled chicken breasts. Foods. 2019;8:616. https://doi.org/10.3390/foods8120616   DOI
28 Sugimura T, Wakabayashi K, Nakagama H, Nagao M. Heterocyclic amines: mutagens/ carcinogens produced during cooking of meat and fish. Cancer Sci. 2004;95:290-9. https://doi.org/10.1111/j.1349-7006.2004.tb03205.x   DOI
29 Zheng W, Lee SA. Well-done meat intake, heterocyclic amine exposure, and cancer risk. Nutr Cancer. 2009;61:437-46. https://doi.org/10.1080/01635580802710741   DOI
30 Oz F, Kaya M. Heterocyclic aromatic amines in meat. J Food Process Preserv. 2011;35:739-53. https://doi.org/10.1111/j.1745-4549.2011.00524.x   DOI
31 Warzecha L, Janoszka B, Blaszczyk U, Strozyk M, Bodzek D, Dobosz C. Determination of heterocyclic aromatic amines (HAs) content in samples of household-prepared meat dishes. J Chromatogr B. 2004;802:95-106. https://doi.org/10.1016/j.jchromb.2003.09.027   DOI
32 Jung DW, Huang YH, Choi GP, Kang IJ. Acute and subchronic toxicity of gammairradiated orange. J Korean Soc Food Sci Nutr. 2015;44:1286-94. https://doi.org/10.3746/jkfn.2015.44.9.1286   DOI
33 Zimmerli B, Rhyn P, Zoller O, Schlatter J. Occurrence of heterocyclic aromatic amines in the Swiss diet: analytical method, exposure estimation and risk assessment. Food Addit Contam. 2001;18:533-51. https://doi.org/10.1080/02652030119545   DOI
34 Knize MG, Dolbeare FA, Cunningham PL, Felton JS. Mutagenic activity and heterocyclic amine content of the human diet. Princess Takamatsu Symp. 1995;23:30-8.
35 Puangsombat K, Gadgil P, Houser TA, Hunt MC, Scott Smith J. Heterocyclic amine content in commercial ready to eat meat products. Meat Sci. 2011;88:227-33. https://doi.org/10.1016/j.meatsci.2010.12.025   DOI
36 Korean Society for Laboratory Medicine. Hematocrit [Internet]. 2017 [cited 2021 Nov 17]. https://labtestsonline.kr/tests/hct
37 Korean Society for Laboratory Medicine. BUN [Internet]. 2017 [cited 2021 Nov 17]. https://labtestsonline.kr/tests/bun
38 Korean Society for Laboratory Medicine. Creatinine [Internet]. 2017 [cited 2021 Nov 17]. https://labtestsonline.kr/tests/creatinine
39 Pourkhalili A, Mirlohi M, Rahimi E. Heme iron content in lamb meat is differentially altered upon boiling, grilling, or frying as assessed by four distinct analytical methods. Sci World J. 2013;2013:374030. https://doi.org/10.1155/2013/374030   DOI
40 Turhan S, Ustun NS, Altunkaynak TB. Effect of cooking methods on total and heme iron contents of anchovy (Engraulis encrasicholus). Food Chem. 2004;88:169-72. https://doi.org/10.1016/j.foodchem.2004.01.026   DOI
41 Derelanko MJ. The toxicologist's pocket handbook. 2nd ed. Boca Raton, FL: CRC Press; 2008.
42 Seo HW, Suh JH, So SH, Kyung JS, Kim YS, Han CK. Subacute oral toxicity and bacterial mutagenicity study of Korean red ginseng oil. J Ginseng Res. 2017;41:595-601. https://doi.org/10.1016/j.jgr.2017.01.009   DOI
43 Danneman PJ, Suckow MA, Brayton C. The laboratory mouse. 1st ed. Boca Raton, FL: CRC Press; 2000.
44 Lee YH, Chung YH, Kim HY, Shin SH, Lee SB. Subacute inhalation toxicity of cyclohexanone in B6C3F1 mice. Toxicol Res. 2018;34:49-53. https://doi.org/10.5487/TR.2018.34.1.049   DOI
45 Jung EY, Lee DY, Kim OY, Lee SY, Yim DG, Hur SJ. Subacute feeding toxicity of lowsodium sausages manufactured with sodium substitutes and biopolymer-encapsulated saltwort (Salicornia herbacea) in a mouse model. J Sci Food Agric. 2020;100:794-802. https://doi.org/10.1002/jsfa.10087   DOI
46 Serfilippi LM, Stackhouse Pallman DR, Russell B, Spainhour CB. Serum clinical chemistry and hematology reference values in outbred stocks of albino mice from three commonly used vendors and two inbred strains of albino mice. J Am Assoc Lab Anim Sci. 2003;42:46-52.
47 Cho J, Kim HJ, Kwon JS, Kim HJ, Jang A. Effect of marination with black currant juice on the formation of biogenic amines in pork belly during refrigerated storage. Food Sci Anim Resour. 2021;41:763-78. https://doi.org/10.5851/kosfa.2021.e34   DOI
48 Widen C, Renvert S, Persson GR. Antibacterial activity of berry juices, an in vitro study. Acta Odontol Scand. 2015;73:539-43. https://doi.org/10.3109/00016357.2014.887773   DOI
49 Jia N, Kong B, Liu Q, Diao X, Xia X. Antioxidant activity of black currant (Ribes nigrum L.) extract and its inhibitory effect on lipid and protein oxidation of pork patties during chilled storage. Meat Sci. 2012;91:533-9. https://doi.org/10.1016/j.meatsci.2012.03.010   DOI
50 Carvalho AM, Miranda AM, Santos FA, Loureiro APM, Fisberg RM, Marchioni DM. High intake of heterocyclic amines from meat is associated with oxidative stress. Br J Nutr. 2015;113:1301-7. https://doi.org/10.1017/S0007114515000628   DOI
51 Ferguson LR. Meat and cancer. Meat Sci. 2010;84:308-13. https://doi.org/10.1016/j.meatsci.2009.06.032   DOI
52 Santarelli RL, Pierre F, Corpet DE. Processed meat and colorectal cancer: a review of epidemiologic and experimental evidence. Nutr Cancer. 2008;60:131-44. https://doi.org/10.1080/01635580701684872   DOI
53 Hayatsu H, Negishi T, Arimoto S, Hayatsu T. Porphyrins as potential inhibitors against exposure to carcinogens and mutagens. Mutat Res. 1993;290:79-85. https://doi.org/10.1016/0027-5107(93)90035-E   DOI
54 Lund MN, Ray CA. Control of Maillard reactions in foods: strategies and chemical mechanisms. J Agric Food Chem. 2017;65:4537-52. https://doi.org/10.1021/acs.jafc.7b00882   DOI
55 Rackauskiene I, Pukalskas A, Venskutonis PR, Fiore A, Troise AD, Fogliano V. Effects of beetroot (Beta vulgaris) preparations on the Maillard reaction products in milk and meatprotein model systems. Food Res Int. 2015;70:31-9. https://doi.org/10.1016/j.foodres.2015.01.026   DOI
56 Son SH, Hong YJ, Han GJ, Yu SM, Yoo SS. Analysis of free sugar and free amino acid from Gochujang produced from Korean small farms. Korean J Food Cook Sci. 2013;29:543-52. https://doi.org/10.9724/kfcs.2013.29.5.543   DOI
57 Kim YS, Song GS. Characteristics of kiwifruit-added traditional kochujang. Korean J Food Sci Technol. 2002;34:1091-7.
58 Lee KG, Shibamoto T. Toxicology and antioxidant activities of non-enzymatic browning reaction products. Food Rev Int. 2002;18:151-75. https://doi.org/10.1081/FRI-120014356   DOI
59 Vitaglione P, Fogliano V. Use of antioxidants to minimize the human health risk associated to mutagenic/carcinogenic heterocyclic amines in food. J Chromatogr B. 2004;802:189-99. https://doi.org/10.1016/j.jchromb.2003.09.029   DOI
60 Hasnol NDS, Jinap S, Sanny M. Effect of different types of sugars in a marinating formulation on the formation of heterocyclic amines in grilled chicken. Food Chem. 2014;145:514-21. https://doi.org/10.1016/j.foodchem.2013.08.086   DOI
61 Park JE, Kim E. Effects of luteolin on chemical induced colon carcinogenesis in high fat dietfed obese mouse. J Nutr Health. 2018;51:14-22. https://doi.org/10.4163/jnh.2018.51.1.14   DOI
62 Eeckhaut V, Machiels K, Perrier C, Romero C, Maes S, Flahou B, et al. Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut. 2013;62:1745-52. https://doi.org/10.1136/gutjnl-2012-303611   DOI
63 Kim DH. Risk factors of colorectal cancer. J Korean Soc Coloproctol. 2009;25:356-62. https://doi.org/10.3393/jksc.2009.25.5.356   DOI
64 Nagao M, Honda M, Seino Y, Yahagi T, Sugimura T. Mutagenicities of smoke condensates and the charred surface of fish and meat. Cancer Lett. 1977;2:221-6. https://doi.org/10.1016/S0304-3835(77)80025-6   DOI
65 Kim DH, Lee JS. Effect of condiments on the physicochemical characteristics of traditional Kochujang during fermentation. Korean J Food Sci Technol. 2001;33:353-60.
66 Sanz Alaejos M, Ayala JH, Gonzalez V, Afonso AM. Analytical methods applied to the determination of heterocyclic aromatic amines in foods. J Chromatogr B. 2008;862:15-42. https://doi.org/10.1016/j.jchromb.2007.11.040   DOI
67 Adeyeye SAO. Heterocyclic amines and polycyclic aromatic hydrocarbons in cooked meat products: a review. Polycycl Aromat Compd. 2020;40:1557-67. https://doi.org/10.1080/10406638.2018.1559208   DOI
68 Lee SY, Yim DG, Lee DY, Kim OY, Kang HJ, Kim HS, et al. Overview of the effect of natural products on reduction of potential carcinogenic substances in meat products. Trends Food Sci Technol. 2020;99:568-79. https://doi.org/10.1016/j.tifs.2020.03.034   DOI
69 Rahman U, Sahar A, Khan MI, Nadeem M. Production of heterocyclic aromatic amines in meat: chemistry, health risks and inhibition. A review. LWT - Food Sci Technol. 2014;59:229-33. https://doi.org/10.1016/j.lwt.2014.06.005   DOI
70 Pouzou JG, Costard S, Zagmutt FJ. Probabilistic assessment of dietary exposure to heterocyclic amines and polycyclic aromatic hydrocarbons from consumption of meats and breads in the United States. Food Chem Toxicol. 2018;114:361-74. https://doi.org/10.1016/j.fct.2018.02.004   DOI
71 Turesky RJ. Formation and biochemistry of carcinogenic heterocyclic aromatic amines in cooked meats. Toxicol Lett. 2007;168:219-27. https://doi.org/10.1016/j.toxlet.2006.10.018   DOI
72 Snyderwine EG, Yu M, Schut HAJ, Knight-Jones L, Kimura S. Effect of CYP1A2 deficiency on heterocyclic amine DNA adduct levels in mice. Food Chem Toxicol. 2002;40:1529-33. https://doi.org/10.1016/S0278-6915(02)00110-2   DOI
73 Myung DS, Joo YE. Gut microbial influence and probiotics on colorectal cancer. Korean J Gastroenterol. 2012;60:275-84. https://doi.org/10.4166/kjg.2012.60.5.275   DOI
74 Choe JH, Yang HS, Lee SH, Go GW. Characteristics of pork belly consumption in South Korea and their health implication. J Anim Sci Technol. 2015;57:22. https://doi.org/10.1186/s40781-015-0057-1   DOI