Thermal stability and digestibility of a biopolymer system for the delivery of minor nutrients in enriched meat products

The study examined thermal stability and digestibility of a biopolymer delivery system for the liposomal form of minor nutrients (omega-3 polyunsaturated fatty acids, vitamin D3, essential oil of clove buds) in enriched meat products. A fraction of encapsulated liposomes in the biopolymer delivery system, i. e. in the supramolecular complex with sodium caseinate (SC), was more than 74%. The difference between the number of bound liposomes before and after freeze-drying is statistically insignificant. The study of the fatty acid composition in samples of enriched meat product containing a supramolecular complex (EPSC) and enriched meat product containing components of the supramolecular complex (EPC) showed that the total omega-3 fatty acids content in EPC was 0.079 ± 0.002 g/100 g, while in EPSC it was 0.207 ± 0.002 g/100 g. The data obtained made it possible to state that EPSC sample was a source of omega-3 fatty acids. Product fortification with the supramolecular complex made it possible to meet the daily requirement of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) by 70%, and vitamin D3 by 470%. A study of the in vitro digestion of EPC and EPSC enriched meat products, it was revealed that in both samples, release of fat in the gastric phase was almost identical, in contrast to the intestinal phase, where the released fat in EPSC was found to be 2 times higher than in EPC. This indicates that the use of physiologically functional ingredients in encapsulated form to fortify meat products is more effective and does not violate the general principles of lipid digestion. At the same time, the mass fraction of released fatty acids in the intestinal phase was higher by 74.4% and 48.5%, respectively, when using physiologically functional ingredients in the form of a supramolecular complex in comparison with a product containing these ingredients in their native form. Use of high temperature treatment did not affect the bioavailability of EPA and DHA, as well as the organoleptic parameters or oxidative stability of EPSC.

1. Serov, V.N., Sidеlnikovа, V.M. (2008). Omega-3 polyunsaturated fatty acids in the practice of an obstetrician-gynecologist. Methodological recommendations for obstetricians-gynecologists and general practitioners. Moscow, 2008. (In Russian)

2. Zhang, T.-T., Xu, J., Wang, Y.-M., Xue, C.-H. (2019). Health benefits of dietary marine DHA/EPA-enriched glycerophospholipids Progress in Lipid Research, 75, Article 100997. https://doi.org/10.1016/j.plipres.2019.100997

3. Zelikina, D. V., Gureeva, M. D., Chebotarev, S. A., Samuseva, Yu. V., Antipova, A. S., Martirosova, E. I. et al. (2020). Functional food compositions based on whey protein isolate, fish oil and soy phospholipids. Food Systems, 3(1), 16–20. https://doi.org/10.21323/2618-9771-2020-3-1-16-20

4. Aquilani, C., T. Pérez-Palacios, T., Sirtori, F., E. Jiménez-Martín, E., Antequera, T., O. Franci, O. et al. (2018). Enrichment of Cinta Senese burgers with omega-3 fatty acids. Effect of type of addition and storage conditions on quality characteristics. Grasas y Aceites, 69(1), Article 235. https://doi.org/10.3989/gya.0671171

5. Solomando, J. С., Vázquez, F., Antequera, T., Folgado, C., Perez-Palacios, T. (2023). Addition of fish oil microcapsules to meat products — Implications for omega-3 enrichment and salt reduction. Journal of Functional Foods, 105, Article 105575. https://doi.org/10.1016/j.jff.2023.105575

6. Bolger, Z., Brunton, N. P., Monahan, F. J. (2017). Effect of mode of addition of flaxseed oil on the quality characteristics of chicken sausage containing Vitamin E and omega 3 fatty acids at levels to support a health claim. Food and Fuction, 8(10), 3563–3575. https://doi.org/10.1039/C7FO00929A

7. Rahim, M. A., Imran, M., Khan, F. A., Al-Asmari, F., Mosa, O. F., Almalki, R. S. et al. (2024). Omega-3-enriched and oxidative stable mayonnaise formulated with spray-dried microcapsules of chia and fish oil blends. ACS Omega, 9(7), 8221–8228. https://doi.org/10.1021/acsomega.3c08807

8. do Prado, G. M., de Sousa, P. H. M., da Silva, L. M. R., Wurlitzer, N. J., Garruti, D. dos S., de Figueiredo, R. W. (2022). Encapsulated omega-3 addition to a cashew apple/ araça-boi juice — effect on sensorial acceptability and rheological properties. Food Science and Technology, 42(2), Article e64321. https://doi.org/10.1590/fst.64321

9. Mohammadi, B., Shekaari, H., Zafarani-Moattar, M. T. (2022). Study of the nano-encapsulated vitamin D3 in the bio-based phase change material: Synthesis and characteristics. Journal of Molecular Liquids, 350, Article 118484. https://doi.org/10.1016/j.molliq.2022.118484

10. Chang, C., Nickerson, M. T. (2018). Encapsulation of omega 3–6–9 fatty acids-rich oils using protein-based emulsions with spray drying. Journal of Food Science and Technology, 55(8), 2850–2861. https://doi.org/10.1007/s13197-018-3257-0

11. Le Priol, L., Gmur, J., Dagmey, A., Morandat, S., Kirat, K. E., Saleh, K. et al. (2022). Oxidative stability of encapsulated sunflower oil: Effect of protein-polysaccharide mixtures and long-term storage. Journal of Food Measurement and Characterization, 16(2), 1483–1493. https://doi.org/10.1007/s11694-021-01254-5

12. Lamazhapova, G.P., Syngeeva, E.V., Kozlova, T.S., Zhamsaranova, S.D. (2017). Development of liposomal form of polyunsaturated fatty acid concentrate: Ways of using in production of functional foods. Voprosy Pitaniia (Problems of Nutrition), 86(1), 76–84. (In Russian)

13. Piwowarczyk, L., Kucinska, M., Tomczak, S., Mlynarczyk, D. T., Piskorz, J., Goslinski, T. et al. (2022). Liposomal nanoformulation as a carrier for curcumin and pEGCG — Study on stability and anticancer potential. Nanomaterials, 12(8), Article 1274. https://doi.org/10.3390/nano12081274

14. Garidel, P., Hildebrand, A., Knauf, K., Blume, A. (2007). Membranolytic activity of bile salts: Influence of biological membrane properties and composition. Molecules, 12(10), 2292–326. https://doi.org/10.3390/12102292

15. Semenova, M., Antipova, A., Martirosova, E., Zelikina, D., Palmina, N., Chebotarev, S. (2021). Essential contributions of food hydrocolloids and phospholipid liposomes to the formation of carriers for controlled delivery of biologically active substances via the gastrointestinal tract. Food Hydrocolloids, 120, Article 106890. https://doi.org/10.1016/j.foodhyd.2021.106890

16. Barbosa-Nuñez, J. A., Espinosa-Andrews, H., Cardona, A. A. V., Haro-González, J. N. (2025). Polymer-based encapsulation in food products: A comprehensive review of applications and advancements. Journal of Future Foods, 5(1), 36–49. https://doi.org/10.1016/j.jfutfo.2024.01.003

17. Morsy, M. K., Elsabagh, R. (2021). Quality parameters and oxidative stability of functional beef burgers fortified with microencapsulated cod liver oil. LWT, 142, Article 110959. https://doi.org/10.1016/j.lwt.2021.110959

18. Jiménez-Martín, E., Antequera Rojas, T., Gharsallaoui, A., Ruiz Carrascal, J., Pérez-Palacios, T. (2016). Fatty acid composition in double and multilayered microcapsules of ω-3 as affected by storage conditions and type of emulsions. Food Chemistry, 194, 476–486. https://doi.org/10.1016/j.foodchem.2015.08.046

19. Solomando, J. C., Antequera, T., González‐Mohíno, A., Perez‐ Palacios, T. (2020). Fish oil/lycopene microcapsules as a source of eicosapentaenoic and docosahexaenoic acids: A case study on spreads. Journal of the Science of Food and Agriculture, 100(5), 1875–1886. https://doi.org/10.1002/jsfa.10188

20. Semenova, M. G., Antipova, A. S., Martirosova, E. I., Chebotarev, S. A., Palmina, N. P., Bogdanova, N. G. et al. (2022). The relationship between the structure and functionality of essential PUFA delivery systems based on sodium caseinate with phosphatidylcholine liposomes without and with a plant antioxidant: An in vitro and in vivo study. Food and Function, 13, 2354–2371. https://doi.org/10.1039/D1FO03336K

21. Semenova, M. G., Antipova, A. S., Martirosova, E. I., Palmina, N. P., Zelikina, D. V., Chebotarev, S. A. et al. (2024). Key structural factors and intermolecular interactions underlying the formation, functional properties and behaviour in the gastrointestinal tract in vitro of the liposomal form of nutraceuticals coated with whey proteins and chitosan. Food and Function, 15(4), 2008–2021. https://doi.org/10.1039/d3fo04285e

22. Barri, A., Ghanbarzadeh, B., Mohammadi, M., Pezeshki, A. (2023). Application of sodium caseinate as protein based coating/stabilizing agent in development and optimization of vitamin D3-loaded nanostructured lipid carriers (NLCs). Food Hydrocolloids, 144, Article 108747. https://doi.org/10.1016/j.foodhyd.2023.108747

23. Brodkorb, A., Egger, L., Alminger, M., Alvito, P., Assunção, R., Ballance, S. et al. (2019). INFOGEST static in vitro simulation of gastrointestinal food digestion. Nature Protocols, 14(4), 991–1014. https://doi.org/10.1038/s41596-018-0119-1

24. Carlos Solomando, J., Vázquez, F., Antequera, T., Folgado, C., Perez-Palacios, T. (2023). Addition of fish oil microcapsules to meat products — Implications for omega-3 enrichment and salt reduction. Journal of Functional Foods, 105, Article 105575. https://doi.org/10.1016/j.jff.2023.105575

25. Kodentsova, V.M., Mendel’, O.I., Khotimchenko, S.A., Baturin, A.K., Nikitiuk, D.B., Tutelyan, V.A. (2017). Physiological needs and effective doses of vitamin D for deficiency correction. Current state of the problem. Pitaniia (Problems of Nutrition), 86(2), 47–62. https://doi.org/10.24411/0042-8833-2017-00033 (In Russian)

26. Rabelo, R. S., Oliveira, I. F., da Silva, V. M., Prata, A. S., Hubinger, M. D. (2018). Chitosan coated nanostructured lipid carriers (NLCs) for loading vitamin D: A physical stability study. International Journal of Biological Macromolecules, 119, 902–912. https://doi.org/10.1016/j.ijbiomac.2018.07.174

27. Solomando, J. C., Antequera, T., Perez-Palacios, T. (2020). Lipid digestion products in meat derivatives enriched with fish oil microcapsules. Journal of Functional Foods, 68, Article 103916. https://doi.org/10.1016/j.jff.2020.103916

28. Wang, L., Zhang, Y., Chen, J.-F., Luo, Y.-Y., Zou, C.-X., Qin, L.-K. et al. (2023). Study on preparation and properties of camellia oleifera seed oil microcapsules by complex coacervation and spray drying. LWT, 184, Article 115056. https://doi.org/10.1016/j.lwt.2023.115056

29. Solomando, J. C., Antequera, T., Ventanas, S., Perez‐Palacios, T. (2021). Sensory profile and consumer perception of meat products enriched with EPA and DHA using fish oil microcapsules. International Journal of Food Science and Technology, 56(6),2926–2937. https://doi.org/10.1111/ijfs.14932