Page Header

Inhibitory Effect of Chlorogenic Acid on Lipid and Protein Oxidation in Rabbit Meat during Cold Storage

Ting Bai, Jiamin Zhang, Yin Zhang, Roungdao Klinjapo, Suvaluk Asavasant, Patchanee Yasurin

Abstract


The application of natural phenolic compounds (NPCs) in the meat industry has attracted increasing attention. In this study, the effects of chlorogenic acid (CGA) at different ratios (0.006% (w/w), 0.01% (w/w), and 0.02% (w/w)) on protein and lipid oxidation in rabbit meat during cold storage at –4 °C were investigated. The results showed that the addition of 0.01% (w/w) CGA significantly reduced protein and lipid oxidation during cold storage. Compared with the control group, the thiobarbituric acid-reactive substances (TBARS) values, lipoxygenase (LOX) activity, and carbonyl content of rabbit meat supplemented with CGA during cold storage were lower, while the sulfhydryl level was higher than that of the control group. Furthermore, a* and a*/b* ratios—which could show the degree of protein oxidation and color stability in meat samples—were positively impacted by CGA. Additionally, it was noted that the addition of CGA lowered the pH and prevented microbes from growing. Therefore, the addition of CGA significantly improved the quality of refrigerated rabbit meat, and the appropriate addition amount of 0.01% CGA (100 mg/kg) means that the CGA cost of 1 kg of meat can be as low as 0.8 yuan, providing a theoretical basis for the application of chlorogenic acid in the meat industry.

Keywords



[1]    T. Imbabi, A. Hassan, O. Ahmed-Farid, O. El-Garhy, I. Sabeq, M. Moustafa, A. Mohammadein, N. Hassan, A. Osman, and M. Sitohy, “Supplementing rabbit diets with butylated hydroxyanisole affects oxidative stress, growth performance, and meat quality,” Animal, vol. 15, no. 9, 2021, Art. no. 100339, doi: 10.1016/j.animal.2021.100339.

[2]    S. Agradi, M. Sulce, L. Menchetti, D. Vigo, M. Castrica, O. Barbato, E. Andoni, A. Quattrone, A. Munga, M. L. Marongiu, G. Curone, and G. Brecchia, “Dietary supplementation with n-3 polyunsaturated fatty acids: Effects on reproductive and productive performance and meat quality in rabbit breeding,” Animal Nutrition, vol. 14, pp. 70–78, 2023, doi: 10.1016/ j.aninu.2023.03.009.

[3]    X. J. Wang, Y. Y. Xia, D. Zhang, Y. B. Shang, and H. J. Li, “Comparison of different deodorization methods for deodorizing rabbit meat,” Modern Food Science and Technology, vol. 32, no. 5, pp. 205–212, 2017, doi: 10.13982/ j.mfst.1673-9078.2016.5.032.

[4]    L. C. C. Magalhaes, R. B. Costa, and G. M. F. de Camargo, “Consumption of rabbit meat in brazil: Potential and limitations,” Meat Science, vol. 191, 2022, Art. no. 108873, doi: 10.1016/j. meatsci.2022.108873.

[5]    Z. Wu, M. Xu, W. He, X. Li, C. Qiu, and J. Zhang, “Unraveling the physicochemical properties and bacterial communities in rabbit meat during chilled storage,” Foods, vol. 13, no. 4, 2024, Art. no. 623, doi: 10.3390/foods13040623.

[6]    X. Xu, A. Liu, S. Hu, I. Ares, M.-R. Martínez-Larrañaga, X. Wang, M. Martínez, A. Anadón, and M.-A. Martínez, “Synthetic phenolic antioxidants: Metabolism, hazards and mechanism of action,” Food Chemisty, vol. 353, 2021, Art. no. 129488, doi: 10.1016/j.foodchem.2021. 129488.

[7]    E. P. Laveriano-Santos, A. López-Yerena, C. Jaime-Rodríguez, J. González-Coria, R. M. Lamuela-Raventós, A. Vallverdú-Queralt, J. Romanyà, and M. Pérez, “Sweet potato is not simply an abundant food crop: A comprehensive review of its phytochemical constituents, biological activities, and the effects of processing,” Antioxidants, vol. 11, no. 9, 2022, Art. no. 1648, doi: 10.3390/antiox11091648.

[8]    X. Chen, W. Lan, and J. Xie, “Natural phenolic compounds: Antimicrobial properties, antimicrobial mechanisms, and potential utilization in the preservation of aquatic products,” Food Chemisty, vol. 440, 2024, Art. no. 138198, doi: 10.1016/j.foodchem.2023.138198.

[9]    N. J. Oswell, H. Thippareddi, and R. B. Pegg, “Practical use of natural antioxidants in meat products in the U.S.: A review,” Meat Science, vol. 145, pp. 469–479, 2018, doi: 10.1016/j.meatsci.2018.07.020.

[10] M. H. Rahman, M. S. Alam, M. M. Monir, and K. Ahmed, “Comprehensive effects of black cumin (Nigella sativa) and synthetic antioxidant on sensory and physicochemical quality of beef patties during refrigerant storage,” Journal of Agriculture and Food Research, vol. 4, 2021, Art. no. 100145, doi: 10.1016/j.jafr.2021.100145.

[11] R. Klinjapo and W. Krasaekoopt, “Application of microencapsulated bamboo leaf extract powder to control the rancidity in moo yor (vietnamese-style sausage) during refrigerated storage,” Applied Science and Engineering Progress, vol. 14, no. 1, pp. 13–18, 2021, doi: 10.14416/j.asep.2020.02.004.

[12] H. A. Al Jumayi, A. Y. Allam, A. E. El-Beltagy, E. H. Algarni, S. F. Mahmoud, and A. A. El Halim Kandil, “Bioactive compound, antioxidant, and radical scavenging activity of some plant aqueous extracts for enhancing shelf life of cold-stored rabbit meat,” Antioxidants (Basel), vol. 11, no. 6, 2022, Art. no. 1056, doi: 10.3390/antiox11061056.

[13] Q. Chen, Z. Wang, H. Li, and B. Xu, “Effects of chitosan-based packaging film crosslinked with nanoencapsulated star anise essential oil and superchilled storage on the quality of rabbit meat patties,” International Journal of Biological Macromolecules, vol. 271, 2024, Art. no. 132402, doi: 10.1016/j.ijbiomac.2024.132402.

[14] C. Dai, H. Li, W. Zhao, Y. Fu, and J. Cheng, “Bioactive functions of chlorogenic acid and its research progress in pig industry,” Journal of Animal Physiology and Animal Nutrition, vol. 108, no. 2, pp. 439–450, 2024, doi: 10.1111/ jpn.13905.

[15] M. Miao and L. Xiang, “Pharmacological action and potential targets of chlorogenic acid,” Advances in Pharmacology, vol. 87, pp. 71–88, 2020, doi: 10.1016/ bs.apha.2019.12.002.

[16] D. Wang, J. Hou, J. Wan, Y. Yang, S. Liu, X. Li, W. Li, X. Dai, P. Zhou, and W. Liu, “Dietary chlorogenic acid ameliorates oxidative stress and improves endothelial function in diabetic mice via nrf2 activation,” Journal of International Medical Research, vol. 49, no. 1, 2021, Art. no. 0300060520985363, doi: 10.1177/030006052098536.

[17] L. Wang, X. Pan, L. Jiang, Y. Chu, S. Gao, X. Jiang, Y. Zhang, Y. Chen, S. Luo, and C. Peng, “The biological activity mechanism of chlorogenic acid and its applications in food industry: A review,” Frontiers in Nutrition, vol. 9, 2022, Art. no. 943911, doi: 10.3389/fnut.2022. 943911.

[18] J. Chen, Z. Song, R. Ji, Y. Liu, H. Zhao, L. Liu, and F. Li, “Chlorogenic acid improves growth performance of weaned rabbits via modulating the intestinal epithelium functions and intestinal microbiota,” Frontiers in Microbiology, vol. 13, 2022, Art. no. 1027101, doi: 10.3389/fmicb. 2022.1027101.

[19] R. Ji, J. Chen, J. Xu, L. Zhang, L. Liu and F. Li, “Protective effect of chlorogenic acid on liver injury in heat‐stressed meat rabbits,” Journal of Animal Physiology and Animal Nutrition, vol. 108, no. 5, pp. 1203–1213, 2024, doi: 10.1111/ jpn.13966.

[20] J. Zou, X. Liu, X. Wang, H. Yang, J. Cheng, Y. Lin, and D. Tang, “Influence of gelatin-chitosan-glycerol edible coating incorporated with chlorogenic acid, gallic acid, and resveratrol on the preservation of fresh beef,” Foods, vol. 11, no. 23, 2022, Art. no. 3813, doi: 10.3390/foods 11233813.

[21] X. Yang, W. Lan, X. Zhao, A. Lang, and J. Xie, “Inhibitory effects of chitosan grafted chlorogenic acid on antioxidase activity, and lipid and protein oxidation of sea bass (Lateolabrax japonicus) fillets stored at 4 °C,” Journal of the Science of Food and Agriculture, vol. 102, no. 14, pp. 6236–6245, 2022, doi: 10.1002/jsfa. 11972.

[22] X. Yang, X. Yang, X. Sun, D. Zhang, X. Gao, and Z. Wang, “Effects of combined chlorogenic acid and cold plasma on the colour and flavour of roasted mutton patties,” International Journal of Food Science & Technology, vol. 58, no. 12, pp. 6563–6575, 2023, doi: 10.1111/ijfs.16770.

[23] M. Muzolf-Panek and A. Kaczmarek, “Chemometric analysis of fatty acid composition of raw chicken, beef, and pork meat with plant extract addition during refrigerated storage,” Molecules, vol. 26, no. 16, 2021, Art. no. 4952, doi: 10.3390/molecules26164952.

[24] J. Cheng, R. Xiang, D. Tang, M. Zhu, and X. Liu, “Regulation of protein oxidation in cantonese sausages by rutin, quercetin and caffeic acid,” Meat Science, vol. 175, 2021, Art. no. 108422, doi: 10.1016/j.meatsci. 2020.108422.

[25] İ. Gülçin, “Antioxidant activity of caffeic acid (3, 4-dihydroxycinnamic acid),” Toxicology, vol. 217, no. 2–3, pp. 213–220, 2006, doi: 10.1016/ j.tox.2005.09.011.

[26] L. Ji, S. Wang, Y. Zhou, Q. Nie, C. Zhou, J. Ning, C. Ren, C. Tang, and J. Zhang, “Effects of saccharomyces cerevisiae and kluyveromyces marxianus on the physicochemical, microbial, and flavor changes of sauce meat during storage,” Foods, vol. 13, no. 3, 2024, Art. no.  396, doi: 10.3390/foods13030396.

[27] R. Cao, L. Yan, S. Xiao, B. Hou, X. Zhou, W. Wang, T. Bai, K. Zhu, J. Cheng, and J. Zhang, “Effects of different low-temperature storage methods on the quality and processing characteristics of fresh beef,” Foods, vol. 12, no. 4, 2023, Art. no. 782, doi: 10.3390/foods12040782.

[28] L. Ji, C. Zhou, Y. Zhou, Q. Nie, Y. Luo, R. Yang, S. Wang, J. Ning, J. Zhang, and Y. Zhang, “Study on simulation effect of physical and chemical characteristics of sausage by sausage model system,” Frontiers in Nutrition, vol. 11, 2024, Art. no. 1408618, doi: 10.3389/fnut.2024.1408618.

[29] E. M. Hussen and S. A. Endalew, “In vitro antioxidant and free-radical scavenging activities of polar leaf extracts of Vernonia amygdalina,” BMC Complementary Medicine and Therapies, vol. 23, no. 146, pp. 1–12, 2023, doi: 10.1186/s12906-023-03923-y.

[30] E. M. Marinova, A. Toneva, and N. Yanishlieva, “Comparison of the antioxidative properties of caffeic and chlorogenic acids,” Food Chemisty, vol. 114, no. 4, pp. 1498–1502, 2009, doi: 10.1016/j.foodchem.2008.11.045.

[31] J. C. Sánchez‐Rangel, D. A. Jacobo‐Velázquez, L. Cisneros‐Zevallos, and J. Benavides, “Primary recovery of bioactive compounds from stressed carrot tissue using aqueous two‐phase systems strategies,” Journal of Chemical Technology & Biotechnology, vol. 91, no. 1, pp. 144–154, 2016, doi: 10.1002/jctb.4553.

[32] M. D. Gamboa, D. M. O. Santiago, A. S. L. Sulabo, and M. A. O. Torio, “Microbiological and physicochemical changes in rabbit meat during ambient storage,” The Philippine Agricultural Scientist,  vol. 107, no. 107, pp. 89–101, 2024, doi: 10.62550/JAB090023.

[33] E. Żelechowska and W. Przybylski, “Effect of feeding season on ph, glycolytic potential, colour and myofibrillar proteins in rabbit meat,” Med Weter, vol. 71, no. 12, pp. 769–772, 2015.

[34] L. M. Carrillo-Lopez, D. Robledo, V. Martínez, M. Huerta-Jimenez, M. Titulaer, A. D. Alarcon-Rojo, A. Chavez-Martinez, L. Luna-Rodriguez, and L. R. Garcia-Flores, “Post-mortem ultrasound and freezing of rabbit meat: Effects on the physicochemical quality and weight loss,” Ultrasonics Sonochemistry, vol. 79, 2021, Art. no. 105766, doi: 10.1016/j.ultsonch.2021.105766.

[35] F. Hulot and J. Ouhayoun, “Muscular ph and related traits in rabbits: A review,” World Rabbit Science, vol. 7, no. 1, pp. 15–36, 1999, doi: 10.4995/wrs.1999.378.

[36] A. I. Ihekoronye and P. O. Ngoody, Integrated Food Science and Technology for the Tropics, Tropical Fruits and Vegetables. London: Macmillan Education Ltd., pp. 332–333, 1985.

[37] S. Mancini, S. Mattioli, R. Nuvoloni, F. Pedonese, A. D. Bosco, and G. Paci, “Effects of garlic powder and salt on meat quality and microbial loads of rabbit burgers,” Foods, vol. 9, no. 8, 2020, Art. no. 1022, doi: 10.3390/foods9081022.

[38] Y. Cao, R. D. Warner, and Z. Fang, “Effect of chitosan/nisin/gallic acid coating on preservation of pork loin in high oxygen modified atmosphere packaging,” Food Control, vol. 101, pp. 9–16, 2019, doi: 10.1016/j.foodcont.2019.02.013.

[39] R. Chug, S. Mathur, S. Kothari, and V. S. Gour, “Maximizing eps production from pseudomonas aeruginosa and its application in cr and ni sequestration,” Biochemistry and Biophysics Reports, vol. 26, 2021, Art. no. 100972, doi: 10.1016/j.bbrep.2021.100972.

[40] N. Mahanta, A. Gupta, and S. Khare, “Production of protease and lipase by solvent tolerant Pseudomonas aeruginosa psea in solid-state fermentation using Jatropha curcas seed cake as substrate,” Bioresource Technology, vol. 99, no. 6, pp. 1729–1735, 2008, doi: 10.1016/ j.biortech.2007.03.046.

[41] M. Papon and R. Talon, “Cell location and partial characterization of Brochothrix thermosphacta and Lactobacillus curvatus lipases,” Journal of Applied Microbiology, vol. 66, no. 3, pp. 235–242, 1989, doi: 10.1111/j.1365-2672.1989.tb02474.x.

[42] T. Bambeni, T. Tayengwa, O. C. Chikwanha, M. Manley, P. A. Gouws, J. Marais, O. A. Fawole, and C. Mapiye, “Biopreservative efficacy of grape (Vitis vinifera) and clementine mandarin orange (Citrus reticulata) by-product extracts in raw ground beef patties,” Meat Science, vol. 181, 2021, Art. no. 108609, doi: 10.1016/j.meatsci. 2021.108609.

[43] K. Śmiecińska, A. Gugołek, and D. Kowalska, “Effects of garlic (allium sativum L.) and ramsons (allium ursinum L.) on lipid oxidation and the microbiological quality, physicochemical properties and sensory attributes of rabbit meat burgers,” Animals, vol. 12, no. 15, 2022, Art. no. 1905, doi: 10.3390/ani 12151905.

[44] Z. Lou, H. Wang, S. Zhu, C. Ma, and Z. Wang, “Antibacterial activity and mechanism of action of chlorogenic acid,” Journal of Food Science, vol. 76, no. 6, pp. 398–403, 2011, doi: 10.1111/ j.1750-3841.2011.02213.x.

[45] M. Lakhani, S. Azim, S. Akhtar, and Z. Ahmad, “Inhibition of Escherichia coli atp synthase and cell growth by dietary pomegranate phenolics,” International Journal of Biological Macromolecules, vol. 213, pp. 195–209, 2022, doi: 10.1016/j. ijbiomac.2022.05.111.

[46] R. Ganhão, M. Estévez, and D. Morcuende, “Suitability of the tba method for assessing lipid oxidation in a meat system with added phenolic-rich materials,” Food Chem, vol. 126, no. 2, pp. 772–778, 2011, doi: 10.1016/j.foodchem.2010. 11.064.

[47] M. Loncaric, I. Strelec, T. Moslavac, D. Subaric, V. Pavic, and M. Molnar, “Lipoxygenase inhibition by plant extracts,” Biomolecules, vol. 11, no. 2, 2021, Art. no. 152, doi: 10.3390/ biom11020152.

[48] Q. Cao, H. Du, Y. Huang, Y. Hu, J. You, R. Liu, S. Xiong, and A. Manyande, “The inhibitory effect of chlorogenic acid on lipid oxidation of grass carp (Ctenopharyngodon idellus) during chilled storage,” Food and Bioprocess Technology, vol. 12, pp. 2050–2061, 2019, doi: 10.1007/ s11947-019-02365-0.

[49] M. Estévez, S. Díaz-Velasco, and R. Martínez, “Protein carbonylation in food and nutrition: A concise update,” Amino Acids, vol. 54, no. 4, pp. 559–573, 2022, doi: 10.1007/s00726-021-03085-6.

[50] E. V. Estrada, N. Zhang, H. Wennerström, J. Danielsson, and M. Oliveberg, “Diffusive intracellular interactions: On the role of protein net charge and functional adaptation,” Current Opinion in Structural Biology, vol. 81, 2023, Art. no. 102625, doi: 10.1016/j.sbi.2023.102625.

[51] A. Ahmad, N. Mahmood, M. Hussain, U. Aiman, S. H. Al-Mijalli, M. A. Raza, and E. Al Jbawi, “Improvement in oxidative stability and quality characteristics of functional chicken meat product supplemented with aqueous coriander extract,” International Journal of Food Properties, vol. 26, no. 1, pp. 855–865, 2023, doi: 10.1080/10942912.2023.2189086.

[52] R. Griffith and E. G. Hammond, “Generation of swiss cheese flavor components by the reaction of amino acids with carbonyl compounds,” Journal of Dairy Science, vol. 72, no. 3, pp. 604–613, 1989, doi: 10.3168/jds.S0022-0302(89)79150-5.

[53] Z. Wang, Z. He, X. Gan, and H. Li, “Interrelationship among ferrous myoglobin, lipid and protein oxidations in rabbit meat during refrigerated and superchilled storage,” Meat Science, vol. 146, pp. 131–139, 2018, doi: 10.1016/j.meatsci.2018.08. 006.

[54] X. Cao, M. N. Islam, B. Chitrakar, Z. Duan, W. Xu, and S. Zhong, “Effect of combined chlorogenic acid and chitosan coating on antioxidant, antimicrobial, and sensory properties of snakehead fish in cold storage,” Food Science & Nutrition, vol. 8, no. 2, pp. 973–981, 2020, doi: 10.1002/fsn3. 1378.

[55] F. Soglia, G. Baldi, and M. Petracci, “Relationship between protein and lipid oxidation in rabbit hind leg meat,”  in Proceedings World Rabbit Congress, 2021, pp. 1–13.

[56] S. M. Bae, M. G. Cho, G. T. Hong, and J. Y. Jeong, “Effect of nacl concentration and cooking temperature on the color and pigment characteristics of presalted ground chicken breasts,” Korean journal for food science of animal resources, vol. 38, no. 2, 2018, Art. no. 417, doi: 10.5851/kosfa.2018.38.2.417.

[57] Z. Wang, J. Tu, H. Zhou, A. Lu, and B. Xu, “A comprehensive insight into the effects of microbial spoilage, myoglobin autoxidation, lipid oxidation, and protein oxidation on the discoloration of rabbit meat during retail display,” Meat Science, vol. 172, 2021, Art. no. 108359, doi: 10.1016/j.meatsci.2020.108359.

[58] E. Y. Youssef, C. E. R. Garcia, and M. Shimokomaki, “Effect of salt on color and warmed over flavor in charqui meat processing,” Brazilian Archives of Biology and Technology, vol. 46, pp. 595–600, 2003, doi: 10.1590/S1516-89132003000400014.

[59] S. Al-Dalali, C. Li, and B. Xu, “Effect of frozen storage on the lipid oxidation, protein oxidation, and flavor profile of marinated raw beef meat,” Food Chemisty, vol. 376, 2022, Art. no. 131881, doi: 10.1016/j.foodchem.2021.131881.

Full Text: PDF

DOI: 10.14416/j.asep.2025.03.003

Refbacks

  • There are currently no refbacks.