Effect of pullulan active packaging, incorporated with silver nanoparticles, on cholesterol oxidation product concentrations in boiler meat during storage
Main Article Content
Keywords
cholesterol, active meat packaging, cardiovascular diseases, broiler meat, pullulan
Abstract
Cholesterol oxidation products (COPs) in meat are thrombogenic, mutagenic, atherogenic, carcinogenic, angiotoxic, and cytotoxic, leading to serious health issues. The formation of COPs in meat is induced by oxidative rancidity due to poor meat processing and packaging techniques. Pullulan active packaging, incorporated with silver nanoparticles (AgNPs), is considered strong and biodegradable with characteristics, such as enhanced light, gas, and moisture barrier, that protect the oxidative rancidity of broiler meat. The current study was performed to determine the impact of pullulan active packaging (T1, T2, T3, and T4) on the formation of COPs in broiler meat during refrigerated storage (7 and 14 days). Pullulan active packaging significantly affected (P < 0.05) the concentrations of A-cholestane (0.63±0.10 ppm) and B-epoxy (0.59±0.33 ppm) COPs whereas A-cholestane (0.634±0.08 ppm) was affected significantly (P < 0.05) by the duration of refrigerated storage (0, 7, and 14 days). Broiler meat treated with pullulan active packaging presented a limited level of oxidative rancidity with minimum concentrations of COPs. The findings revealed that broiler meat treated with pullulan active packaging, incorporated with AgNPs, is safer than raw meat for shorter (7 days) and longer (14 days) storage periods at 4±1°C.
References
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Derewiaka, D., and Lorenzo, J.M. 2022. Cholesterol and cholesterol oxidation products (COPs). In: Food lipids. Academic Press, Cambridge, MA, pp. 173–205.
Echegoyen Y., Nerín C. 2013. Nanoparticle release from nano-silver antimicrobial food containers. Food Chemical Toxicology 62:16–22. 10.1016/j.fct.2013.08.014
Gallocchio, F., Cibin V., Biancotto, G., Roccato, A., Muzzolon, O., Carmen, L., et al. 2016. Testing nano-silver food packaging to evaluate silver migration and food spoilage bacteria on chicken meat. Food Additive and Contaminants. Part A Chemistry, Analysis, Control, Exposure & Risk Assessment 33:1063–1071. 10.1080/19440049.2016.1179794
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Khan, M.I., Min, J.-S., Lee, S.-O., Yim, D.G., Seol, K.-H., Lee, M., et al. 2015. Cooking, storage, and reheating effect on the formation of cholesterol oxidation products in processed meat products. Lipids Health Diseases 14(1): 89. 10.1186/s12944-015-0091-5
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Khan, M.J., Shameli, K., Sazili, A., Selamat, J., and Kumari, S. 2019. Rapid green synthesis and characterization of silver nanoparticles arbitrated by curcumin in an alkaline medium. Molecules 24(719): 1–12. 10.3390/molecules24040719
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Liu, Y., Liu, Y., Han, K., Cai, Y., Ma, M., Tong, Q., et al. 2019. Effect of nano-TiO2 on the physical, mechanical and optical properties of pullulan film. Carbohydrate Polymers 218: 95–102. 10.1016/J.CARBPOL.2019.04.073
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Manzoor, S., Masoodi, F.A., Rashid, R., Naqash, F., and Ahmad, M. 2022. Oleogels for the development of healthy meat products: a review. Applied Food Research 2(2): 100212. 10.1016/j.afres.2022.100212
Milićević D, Vranić D, Mašić Z, Parunović N, Trbović D, Nedeljković-Trailović J., et al. 2014. The role of total fats, saturated/unsaturated fatty acids and cholesterol content in chicken meat as cardiovascular risk factors. Lipids Health Diseases 13(1): 42. 10.1186/1476-511X-13–42
Min, J.S., Lee, S.O., Khan, M.I., Yim, D.G., Seol, K.H., Lee, M., et al. 2015. Monitoring the formation of cholesterol oxidation products in model systems using response surface methodology. Lipids in Health and disease, 14: 77. 10.1186/s12944-015-0074-6
Ming-Min, W., and Ismail-Fitry, M.R. 2023. Physicochemical, rheological and microstructural properties of chicken meat emulsion with the addition of Chinese yam (Dioscorea polystachya) and arrowroot (Maranta arundinacea) as meat substitutes. Future Foods 7: 100221. 10.1016/j.fufo.2023.100221
Mir, N.A., Rafi, A., Kumar, F., Singh, V., and Shukla, V. 2017. Determinants of broiler chicken meat quality and factors affecting them : a review. Journal of Food Science Technology 54(10): 2997–3009. 10.1007/s13197-017-2789-z
Mohammed, A.E., Bazargani-Gilani, A.B., and Obaid Hasson, S. 2023. Comparison of green and synthetic silver nanoparticles in zein-based edible films: shelf-life study of cold-stored Turkey breasts. Food Science & Nutrition 11(11): 7352–7363. 10.1002/fsn3.3661
Morsy, M.K., Khalaf, H.H., Sharoba, A.M., El-Tanahi, H.H., and Cutter, C.N. 2014. Incorporation of essential oils and nanoparticles in pullulan films to control foodborne pathogens on meat and poultry products. Journal of Food Science 79(4): M675–M684. 10.1111/1750-3841.12400
Mousavi Khaneghah, A., Hashemi, S.M.B., and Limbo, S. 2018. Antimicrobial agents and packaging systems in antimicrobial active food packaging: an overview of approaches and interactions. Food and Bioproducts Processing 111: 1–19. 10.1016/j.fbp.2018.05.001
Nadia, H. 2019. Cholesterol oxidation products (COPs ) in ruminant meat : a biological and pathological approach : a review. Asian Journal of Dairy and Food Research 38(3): 191–202. 10.18805/ajdfr.DR-134
Noor, S., Bhat, Z.F., Kumar, S., and Mudiyanselage, R.J. 2018. Preservative effect of Asparagus racemosus : a novel additive for bioactive edible films for improved lipid oxidative stability and storage quality of meat products. Meat Science 139(1): 207–212. 10.1016/j.meatsci.2018.02.001
Rahim, A.A., Fahmi, M.I., Hashari, S.Z., and Thema Juhana, M.J. 2012. Detection of cholesterol oxidation products (COPs) in raw and chilled storage of chicken sausages formulated with chicken fat and red palm mid fraction. World Applied Sciences Journal 17: 51–56.
Rai, M., Wypij, M., Ingle, A.P., Trzcińska-Wencel, J., and Golińska, P. 2021. Emerging trends in pullulan-based antimicrobial systems for various applications. International Journal of Molecular Sciences 22(24): 13596. 10.3390/ijms222413596
Ramiah, S.K., Meng, G.Y., and Ebrahimi, M. 2014. Dietary conjugated linoleic acid alters oxidative stability and alleviates plasma cholesterol content in meat of broiler chickens. The Scientific World Journal, 2014: 949324. 10.1155/2014/949324
Rather, S.A., Masoodi, F.A., Rather, J.A., Gani, A., Wani, S.M., Ganaie, T.A., et al. 2021. Impact of thermal processing and storage on fatty acid composition and cholesterol oxidation of canned traditional low-fat meat product of India. Food Science and Technology (LWT) 139: 110503. 10.1016/j.lwt.2020.110503
Serra, A., Conte, G., Cappucci, A., Casarosa, L., Serra, A., Conte, G., et al. 2014. Cholesterol and fatty acids oxidation in meat from three muscles of massese suckling lambs slaughtered at different weights. Italian Journal of Animal Science 13(3275): 648–652. 10.4081/ijas.2014.3275
Synowiec, A., Gniewosz, M., Kraśniewska, K., Przybył, J.L., Bączek, K., and Węglarz, Z. 2014. Antimicrobial and antioxidant properties of pullulan film containing sweet basil extract and an evaluation of coating effectiveness in the prolongation of the shelf life of apples stored in refrigeration conditions. Innovative Food Science and Emerging Technologies 23: 171–181. 10.1016/j.ifset.2014.03.006
Trinetta, V., and Cutter, C.N. 2016. Pullulan: a suitable biopolymer for antimicrobial food packaging applications. In: Barros-Velázquez, J. (ed.) Antimicrobial food packaging. Elsevier, Penn State, State College, PA, pp. 385–397. 10.1016/B978-0-12-800723-5.00030-9
Winiarska-Mieczan, A., Kwiecien, M., Grela, E.R., Tomaszewska, E., and Klebaniuk, R. 2016. The chemical composition and sensory properties of raw , cooked and grilled thigh meat of broiler chickens fed with Fe-Gly chelate. Journal of Food Science and Technology 53(10): 3825–3833. 10.1007/s13197-016-2374-x
Xu, L., and Porter, N.A. 2015. Free radical oxidation of cholesterol and its precursors: implications in cholesterol biosynthesis disorders. Free Radical Research 49(7): 835–849. 10.3109/10715762.2014.985219
Yao, Y., Liu, Y., Li, C., Huang, X., Zhang, X., Deng, P., et al. 2018. Effects of rosemary extract supplementation in feed on growth performance, meat quality, serum biochemistry, antioxidant capacity, and immune function of meat ducks. Poultry Science 102(2): 10235. 10.1016/j.psj.2022.102357
Zerbinati, C., and Iuliano, L. 2017. Cholesterol and related sterols autoxidation. Free Radical Biology and Medicine 111: 151–155. 10.1016/j.freeradbiomed.2017.04.013
Ali, S., Zhang, W., Rajput, N., Khan, M.A., Li, C.B., and Zhou, G.H. 2015. Effect of multiple freeze-thaw cycles on the quality of chicken breast meat. Food Chemistry 173: 808–814. 10.1016/j.foodchem.2014.09.095
Barbaro, A. 2022. Thinking about the future of food safety—a foresight report. Food and Agriculture Organization of the United Nations (FAO), Rome, Italy. Available at: https://www.fao.org/3/cb8667en/cb8667en.pdf (Accessed 1 April 2024).
Bennato, F., Luca, A. Di, Martino, C., Ianni, A., Marone, E., Grotta, L., and Martino, G. 2020. Influence of grape pomace intake on nutritional value, lipid oxidation and volatile profile of poultry meat. Foods 9: 508. 10.3390/foods9040508
Choe, J., Min, J.S., Lee, S.O., Khan, M.I., and Yim, D.G. 2018. Influence of cooking , storage period , and re-heating on production of cholesterol oxides in chicken meat. Korean Journal Food Science of Animal Resources 38(3): 433–441.
Derewiaka, D., and Lorenzo, J.M. 2022. Cholesterol and cholesterol oxidation products (COPs). In: Food lipids. Academic Press, Cambridge, MA, pp. 173–205.
Echegoyen Y., Nerín C. 2013. Nanoparticle release from nano-silver antimicrobial food containers. Food Chemical Toxicology 62:16–22. 10.1016/j.fct.2013.08.014
Gallocchio, F., Cibin V., Biancotto, G., Roccato, A., Muzzolon, O., Carmen, L., et al. 2016. Testing nano-silver food packaging to evaluate silver migration and food spoilage bacteria on chicken meat. Food Additive and Contaminants. Part A Chemistry, Analysis, Control, Exposure & Risk Assessment 33:1063–1071. 10.1080/19440049.2016.1179794
Hashari, S.Z., Rahim, A.A., Meng, G.Y., and Ramiah, S.K. 2020. Quantification of cooking method effect on COP content in meat types using triple quadrupole GC-MS/MS. Molecules 25(21), 4978. 10.3390/molecules25214978
Khan, M.J., Kumari, S., Selamat, J., Shameli, K., and Sazili, A.Q. 2020. Reducing meat perishability through pullulan active packaging. Journal of Food Quality, 2020: 8880977. 10.1155/2020/8880977
Khan, M.J., Kumari, S., Shameli, K., Selamat, J., and Sazili, A.Q. 2019. Green synthesis and characterization of pullulan-mediated silver nanoparticles through ultraviolet irradiation. Materials 12(2382): 1–12. doi:10.3390/ma12152382.
Khan, M.I., Min, J.-S., Lee, S.-O., Yim, D.G., Seol, K.-H., Lee, M., et al. 2015. Cooking, storage, and reheating effect on the formation of cholesterol oxidation products in processed meat products. Lipids Health Diseases 14(1): 89. 10.1186/s12944-015-0091-5
Khan, M.J., Ramiah, S.K., Selamat, J., Sazili, A.Q., and Mookiah, S. 2022. Utilisation of pullulan active packaging incorporated with curcumin and pullulan-mediated silver nanoparticles to maintain the quality and shelf life of broiler meat. Italian Journal of Animal Science 21(1): 244–262. 10.1080/1828051X.2021.2012285
Khan, M.J., Shameli, K., Sazili, A., Selamat, J., and Kumari, S. 2019. Rapid green synthesis and characterization of silver nanoparticles arbitrated by curcumin in an alkaline medium. Molecules 24(719): 1–12. 10.3390/molecules24040719
Li, L.H., Dutkiewicz, E.P., Huang, Y.C., Zhou, H.B., and Hsu, C.C. 2019. Analytical methods for cholesterol quantification. Journal of Food and Drug Analysis 27(2): 375–386. 10.1016/j.jfda.2018.09.001
Liu, Y., Liu, Y., Han, K., Cai, Y., Ma, M., Tong, Q., et al. 2019. Effect of nano-TiO2 on the physical, mechanical and optical properties of pullulan film. Carbohydrate Polymers 218: 95–102. 10.1016/J.CARBPOL.2019.04.073
Macho-González, A., Bastida, S., Garcimartín, A., López-Oliva, M., González, P., Benedí, J., et al. 2021. Functional meat products as oxidative stress modulators: A review. Advances in Nutrition 12(4): 1514–1539. 10.1093/advances/nmaa182
Manzoor, S., Masoodi, F.A., Rashid, R., Naqash, F., and Ahmad, M. 2022. Oleogels for the development of healthy meat products: a review. Applied Food Research 2(2): 100212. 10.1016/j.afres.2022.100212
Milićević D, Vranić D, Mašić Z, Parunović N, Trbović D, Nedeljković-Trailović J., et al. 2014. The role of total fats, saturated/unsaturated fatty acids and cholesterol content in chicken meat as cardiovascular risk factors. Lipids Health Diseases 13(1): 42. 10.1186/1476-511X-13–42
Min, J.S., Lee, S.O., Khan, M.I., Yim, D.G., Seol, K.H., Lee, M., et al. 2015. Monitoring the formation of cholesterol oxidation products in model systems using response surface methodology. Lipids in Health and disease, 14: 77. 10.1186/s12944-015-0074-6
Ming-Min, W., and Ismail-Fitry, M.R. 2023. Physicochemical, rheological and microstructural properties of chicken meat emulsion with the addition of Chinese yam (Dioscorea polystachya) and arrowroot (Maranta arundinacea) as meat substitutes. Future Foods 7: 100221. 10.1016/j.fufo.2023.100221
Mir, N.A., Rafi, A., Kumar, F., Singh, V., and Shukla, V. 2017. Determinants of broiler chicken meat quality and factors affecting them : a review. Journal of Food Science Technology 54(10): 2997–3009. 10.1007/s13197-017-2789-z
Mohammed, A.E., Bazargani-Gilani, A.B., and Obaid Hasson, S. 2023. Comparison of green and synthetic silver nanoparticles in zein-based edible films: shelf-life study of cold-stored Turkey breasts. Food Science & Nutrition 11(11): 7352–7363. 10.1002/fsn3.3661
Morsy, M.K., Khalaf, H.H., Sharoba, A.M., El-Tanahi, H.H., and Cutter, C.N. 2014. Incorporation of essential oils and nanoparticles in pullulan films to control foodborne pathogens on meat and poultry products. Journal of Food Science 79(4): M675–M684. 10.1111/1750-3841.12400
Mousavi Khaneghah, A., Hashemi, S.M.B., and Limbo, S. 2018. Antimicrobial agents and packaging systems in antimicrobial active food packaging: an overview of approaches and interactions. Food and Bioproducts Processing 111: 1–19. 10.1016/j.fbp.2018.05.001
Nadia, H. 2019. Cholesterol oxidation products (COPs ) in ruminant meat : a biological and pathological approach : a review. Asian Journal of Dairy and Food Research 38(3): 191–202. 10.18805/ajdfr.DR-134
Noor, S., Bhat, Z.F., Kumar, S., and Mudiyanselage, R.J. 2018. Preservative effect of Asparagus racemosus : a novel additive for bioactive edible films for improved lipid oxidative stability and storage quality of meat products. Meat Science 139(1): 207–212. 10.1016/j.meatsci.2018.02.001
Rahim, A.A., Fahmi, M.I., Hashari, S.Z., and Thema Juhana, M.J. 2012. Detection of cholesterol oxidation products (COPs) in raw and chilled storage of chicken sausages formulated with chicken fat and red palm mid fraction. World Applied Sciences Journal 17: 51–56.
Rai, M., Wypij, M., Ingle, A.P., Trzcińska-Wencel, J., and Golińska, P. 2021. Emerging trends in pullulan-based antimicrobial systems for various applications. International Journal of Molecular Sciences 22(24): 13596. 10.3390/ijms222413596
Ramiah, S.K., Meng, G.Y., and Ebrahimi, M. 2014. Dietary conjugated linoleic acid alters oxidative stability and alleviates plasma cholesterol content in meat of broiler chickens. The Scientific World Journal, 2014: 949324. 10.1155/2014/949324
Rather, S.A., Masoodi, F.A., Rather, J.A., Gani, A., Wani, S.M., Ganaie, T.A., et al. 2021. Impact of thermal processing and storage on fatty acid composition and cholesterol oxidation of canned traditional low-fat meat product of India. Food Science and Technology (LWT) 139: 110503. 10.1016/j.lwt.2020.110503
Serra, A., Conte, G., Cappucci, A., Casarosa, L., Serra, A., Conte, G., et al. 2014. Cholesterol and fatty acids oxidation in meat from three muscles of massese suckling lambs slaughtered at different weights. Italian Journal of Animal Science 13(3275): 648–652. 10.4081/ijas.2014.3275
Synowiec, A., Gniewosz, M., Kraśniewska, K., Przybył, J.L., Bączek, K., and Węglarz, Z. 2014. Antimicrobial and antioxidant properties of pullulan film containing sweet basil extract and an evaluation of coating effectiveness in the prolongation of the shelf life of apples stored in refrigeration conditions. Innovative Food Science and Emerging Technologies 23: 171–181. 10.1016/j.ifset.2014.03.006
Trinetta, V., and Cutter, C.N. 2016. Pullulan: a suitable biopolymer for antimicrobial food packaging applications. In: Barros-Velázquez, J. (ed.) Antimicrobial food packaging. Elsevier, Penn State, State College, PA, pp. 385–397. 10.1016/B978-0-12-800723-5.00030-9
Winiarska-Mieczan, A., Kwiecien, M., Grela, E.R., Tomaszewska, E., and Klebaniuk, R. 2016. The chemical composition and sensory properties of raw , cooked and grilled thigh meat of broiler chickens fed with Fe-Gly chelate. Journal of Food Science and Technology 53(10): 3825–3833. 10.1007/s13197-016-2374-x
Xu, L., and Porter, N.A. 2015. Free radical oxidation of cholesterol and its precursors: implications in cholesterol biosynthesis disorders. Free Radical Research 49(7): 835–849. 10.3109/10715762.2014.985219
Yao, Y., Liu, Y., Li, C., Huang, X., Zhang, X., Deng, P., et al. 2018. Effects of rosemary extract supplementation in feed on growth performance, meat quality, serum biochemistry, antioxidant capacity, and immune function of meat ducks. Poultry Science 102(2): 10235. 10.1016/j.psj.2022.102357
Zerbinati, C., and Iuliano, L. 2017. Cholesterol and related sterols autoxidation. Free Radical Biology and Medicine 111: 151–155. 10.1016/j.freeradbiomed.2017.04.013
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