Risks of reducing safety of cheese-making products depending on the composition of antibiotics in milk
https://doi.org/10.21323/2618-9771-2026-9-2-199-207
Abstract
The study is aimed at assessing risks of reducing the safety of semi-hard and soft cheeses during processing of milk containing residual amounts of antibiotics. Using the method of model production, the effect of six classes of antibiotics on the development of starter microflora and their distribution between the cheese dough and cheese whey in the technologies of Gollandsky and Adygeysky cheeses was studied. In order to make the analysis results informative, the amount of added antibiotics significantly exceeded the level standardized in raw milk: ampicillin – 35.0 mcg/kg; tetracycline – 250.0 mcg/kg; chlortetracycline – 250.0 mcg/kg; doxytetracycline – 250.0 mcg/kg; streptomycin – 4000.0 mcg/kg; ciprofloxacin – 50.0 mcg/kg; erythromycin – 2500.0 mcg/kg; chloramphenicol – 200.0 mcg/kg. Ampicillin was found to have the most pronounced bactericidal effect, leading to critical suppression of the starter microbiome. Streptomycin, erythromycin, and tetracycline exhibit moderate inhibition, while ciprofloxacin and chloramphenicol have no significant effect on starter cultures. Analysis of the proportional distribution of antibiotics from various groups showed that most of the studied antibiotics are predominantly transferred to the whey (at a level of 85–89 %), which corresponds to the whey-cheese mass distribution. The exception is tetracycline, up to 35 % of which is transferred to the cheese mass. The type of cheese is noted to be one of the determining factors for the final antibiotic content. In Gollandsky cheese, 50–55 % of tetracycline antibiotics (tetracycline, chlortetracycline, and doxytetracycline) accumulate in the cheese dough, posing a direct threat to consumers. In Adygeysky cheese, 81–88 % of the studied antibiotics migrate into the whey, which reduces the load on the cheese but leads to by-product contamination and poses a problem for whey recycling. The experimental data obtained highlight the need to consider not only the initial concentration of antibiotics in milk, but also their nature and the process parameters of cheese production when developing cheese safety management systems.
About the Authors
G. M. SviridenkoRussian Federation
Galina M. Sviridenko, Doctor of Technical Sciences
19, Krasnoarmeysky Boulevard, Uglich, 152613, Yaroslavl Region
M. B. Zakharova
Russian Federation
Marina B. Zakharova, Candidate of Technical Sciences, Researcher, Department of Microbiological Research
19, Krasnoarmeysky Boulevard, Uglich, 152613, Yaroslavl Region
D. S. Mamykin
Russian Federation
Denis S. Mamykin, Candidate of Technical Sciences, Researcher, Department of Microbiological Research
19, Krasnoarmeysky Boulevard, Uglich, 152613, Yaroslavl Region
References
1. Sheveleva, S. A., Bessonov, V. V. (2016). Items of normalization and control of antibiotics in milk, milk products and other products of animal breeding. Dairy Industry, 5, 32–36. (In Russian)
2. Virto, M., Santamarina-García, G., Amores, G., Hernández, I. (2022). Antibiotics in dairy production: Where is the problem? Dairy, 3, 541–564.
3. Van Boeckel, T. P., Brower, C., Gilbert, M., Grenfell, B. T., Levin, S. A., Robinson, T. P. et al. (2015). Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences, 112(18), 5649–5654. https://doi.org/10.1073/pnas.1503141112
4. Landers, T. F., Cohen, B., Wittum, T. E., Larson, E. L. (2012). A review of antibiotic use in food animals: Perspective, policy, and potential. Public Health Reports, 127(1), 4–22. https://doi.org/10.1177/003335491212700103
5. Rajala-Schultz, P., Nødtvedt, A., Halasa, T., Persson Waller, K. (2021). Prudent use of antibiotics in dairy cows: The nordic approach to udder health. Frontiers in Veterinary Science, 8, Article 623998. https://doi.org/10.3389/fvets.2021.623998
6. Fatemi, F., Alizadeh Sani, M., Noori, S. M. A., Hashemi, M. (2023). Status of antibiotic residues in milk and dairy products of Iran: A systematic review and meta-analysis. Journal of Environmental Health Science and Engineering, 22, 31–51. https://doi.org/10.1007/s40201-023-00889-4
7. Yurova, E. A., Meldenberg, D. N., Jyjyn, N. A. (2019). Distribution of the residual quantity of antibiotics in the course of the technological process. Dairy Industry, 2, 26–27. (In Russian)
8. Sachi, S., Ferdous, J., Sikder, M. H., Hussani, S. M. A. K. (2019). Antibiotic residues in milk: Past, present, and future. Journal of Advanced Veterinary and Animal Research, 6(3), 315–332. https://doi.org/10.5455/javar.2019.f350
9. Pol, M., Ruegg, P. L. (2007). Treatment practices and quantification of antimicrobial drug usage in conventional and organic dairy farms in Wisconsin. Journal of Dairy Science, 90(1), 249–261. https://doi.org/10.3168/jds.S0022-0302(07)72626-7
10. de Albuquerque Fernandes, F. A., Magnavita, A. P. A., Ferrao, S. P. B., Gualberto, S. A., Faleiro, A. S., Figueiredo, A. J. et al. (2014). Daily ingestion of tetracycline residue present in pasteurized milk: A public health problem. Environmental Science and Pollution Research, 21(5), 3427–3434. https://doi.org/10.1007/s11356-013-2286-5
11. Quintanilla, P., Doménech, E., Escriche, I., Beltrán, M. C., Molina, M. P. (2019). Food safety margin assessment of antibiotics: Pasteurized goat’s milk and fresh cheese. Journal of Food Protection, 82(9), 1553–1559. https://doi.org/10.4315/0362–028X.JFP-18-434
12. European Centre for Disease Prevention and Control, European Food Safety Authority, European Medicines Agency. (2021). Third joint inter-agency report on integrated analysis of consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals in the EU/EEA. EFSA Journal, 19(6), Article e06712. https://doi.org/10.2903/j.efsa.2021.6712
13. Lu, G., Chen, Q., Li, Y., Liu, Y., Zhang, Y., Huang, Y. et al. (2021). Status of antibiotic residues and detection techniques used in Chinese milk: A systematic review based on cross-sectional surveillance data. Food Research International, 147, Article 110450. https://doi.org/10.1016/j.foodres.2021.110450
14. Treiber, F. M., Beranek-Knauer, H. (2021). Antimicrobial residues in food from animal origin — A review of the literature focusing on products collected in stores and markets worldwide. Antibiotics, 10(5), Article 534. https://doi.org/10.3390/antibiotics10050534
15. Tiseo, K., Huber, L., Gilbert, M., Robinson, T. P., Van Boeckel, T. P. (2020). Global trends in antimicrobial use in food animals from 2017 to 2030. Antibiotics, 9(12), Article 918. https://doi.org/10.3390/antibiotics9120918
16. Zaytseva, N. V., Tutelyan, V. A., Shur, P. Z., Khotimchenko, S. A., Sheveleva, S. A. (2014). Experience of justification of hygienic standards of food safety with the use of criteria for the risk for population health. Hygiene and Sanitation, 93(5), 70–74. (In Russian)
17. Hassan, H. F., Saidy, L., Haddad, R., Hosri, C., Asmar, S., Jammoul, A. et al. (2021). Investigation of the effects of some processing conditions on the fate of oxytetracycline and tylosin antibiotics in the making of commonly consumed cheeses from the East Mediterranean. Veterinary World, 14(6), 1644–1649. https://doi.org/10.14202/vetworld.2021.1644-1649
18. Tian, L., Khalil, S., Bayen, S. (2017). Effect of thermal treatments on the degradation of antibiotic residues in food. Critical Reviews in Food Science and Nutrition, 57(17), 3760–3770. https://doi.org/10.1080/10408398.2016.1164119
19. Grunwald, L., Petz, M. (2003). Food processing effects on residues: Penicillins in milk and yoghurt. Analytica Chimica Acta, 483(1–2), 73–79. https://doi. org/10.1016/S0003-2670(02)01405-8
20. Quintanilla, P., Beltrán, M. C., Molina, A., Escriche, I., Molina, M. P. (2019). Characteristics of ripened Tronchón cheese from raw goat milk containing legally admissible amounts of antibiotics. Journal of Dairy Science, 102(4), 2941–2953. https://doi.org/10.3168/jds.2018-15532
21. Gajda, A., Nowacka-Kozak, E., Gbylik-Sikorska, M., Posyniak, A. (2018). Tetracycline antibiotics transfer from contaminated milk to dairy products and the effect of the skimming step and pasteurisation process on residue concentrations. Food Additives and Contaminants: Part A, 35(1), 66–76. https://doi.org/10.1080/19440049.2017.1397773
22. Hakk, H., Shappell, N. W., Lupton, S. J., Shelver, W. L., Fanaselle, W., Oryang, D. et al. (2016). Distribution of animal drugs between skim milk and milk fat fractions in spiked whole milk: Understanding the potential impact on commercial milk products. Journal of Agricultural and Food Chemistry, 64(1), 326–335. https://doi.org/10.1021/acs.jafc.5b04726
23. Ziv, G., Rasmussen, F. (1975). Distribution of labeled antibiotics in different components of milk following intramammary and intramuscular administrations. Journal of Dairy Science, 58(6), 938–946. https://doi.org/10.3168/jds. S0022-0302(75)84660-1
24. Sniegocki, T., Gbylik-Sikorska, M., Posyniak, A. (2015). Transfer of chloramphenicol from milk to commercial dairy products — experimental proof. Food Control, 57, 411–418. https://doi.org/10.1016/j.foodcont.2015.04.028
25. Cayle, T., Guth, J. H., Hynes, J. T., Kolen, E. P., Stern, M. L. (1986). Penicillin distribution during cheese manufacture and membrane treatment of whey. Journal of Food Protection, 49(10), 796–798. https://doi.org/10.4315/0362-028X‑49.10.796
26. Shappell, N. W., Shelver, W. L., Lupton, S. J., Fanaselle, W., Doren, J. M., Hakk, H. (2017). Distribution of animal drugs among curd, whey, and milk protein fractions in spiked skim milk and whey. Journal of Agricultural and Food Chemistry, 65(4), 938–949. https://doi.org/10.1021/acs.jafc.6b04258
27. Gbylik-Sikorska, M., Gajda, A., Nowacka-Kozak, E., Posyniak, A. (2021). The “force” of cloxacillin residue will be with you in various dairy products — The last experimental evidence. Food Control, 121, Article 107628. https://doi.org/10.1016/j.foodcont.2020.107628
28. Lanyi, K., Darnay, L., Laszlo, N., Lehel, J., Friedrich, L., Győri, R. et al. (2022). Transfer of certain beta-lactam antibiotics from cow’s milk to fresh cheese and whey. Food Additives and Contaminants: Part A, 39(1), 52–60. https://doi.org/10.1080/19440049.2021.1973114
29. Cabizza, R., Rubattu, N., Salis, S., Pes, M., Comunian, R., Paba, A. et al. (2017). Transfer of oxytetracycline from ovine spiked milk to whey and cheese. International Dairy Journal, 70, 12–17. https://doi.org/10.1016/j.idairyj.2016.12.002
30. Cabizza, R., Rubattu, N., Salis, S., Pes, M., Comunian, R., Paba, A. et al. (2018). Impact of a thermisation treatment on oxytetracycline spiked ovine milk: Fate of the molecule and technological implications. LWT, 96, 236–243. https://doi.org/10.1016/j.lwt.2018.05.026
31. Giraldo, J., Althaus, R. L., Beltrán, M. C., Molina, M. P. (2017). Antimicrobial activity in cheese whey as an indicator of antibiotic drug transfer from goat milk. International Dairy Journal, 69, 40–44. https://doi.org/10.1016/j.idairyj.2017.02.003
32. Quintanilla, P., Beltrán, M. C., Molina, M. P., Escriche, I. (2021). Enrofloxacin treatment on dairy goats: Presence of antibiotic in milk and impact of residue on technological process and characteristics of mature cheese. Food Control, 123, Article 107762. https://doi.org/10.1016/j.foodcont.2020.107762
33. Castrica, M., Rebucci, R., Giromini, C., Tretola, M., Cattaneo, D., Baldi, A. (2019). Total phenolic content and antioxidant capacity of agri-food waste and by-products. Italian Journal of Animal Science, 18(1), 336–341. https://doi.org/10.1080/1828051X.2018.1529544
34. Lupton, S. J., Shappell, N. W., Shelver, W. L., Hakk, H. (2018). Distribution of spiked drugs between milk fat, skim milk, whey, curd, and milk protein fractions: Expansion of partitioning models. Journal of Agricultural and Food Chemistry, 66(1), 306–314. https://doi.org/10.1021/acs.jafc.7b04463
35. Cerkvenik, V., Perko, B., Rogelj, I., Doganoc, D. Z., Skubic, V., Beek, W. M. et al. (2004). Fate of ivermectin residues in ewes’ milk and derived products. Journal of Dairy Research, 71(1), 39–45. https://doi.org/10.1017/S0022029903006381
36. Niu, C., Yan, M., Yao, Z., Dou, J. (2023). Antibiotic residues in milk and dairy products in China: Occurrence and human health concerns. Environmental Science and Pollution Research, 30(53), 113138–113150. https://doi.org/10.1007/s11356-023-30312-2
37. Iezzi, S., Lifschitz, A., Sallovitz, J., Nejamkin, P., Lloberas, M., Manazza, J. et al. (2014). Closantel plasma and milk disposition in dairy goats: Assessment of drug residues in cheese and ricotta. Journal of Veterinary Pharmacology and Therapeutics, 37(6), 589–594. https://doi.org/10.1111/jvp.12135
38. Stefańska, I., Kwiecień, E., Jóźwiak-Piasecka, K., Garbowska, M., Binek, M., Rzewuska, M. (2021). Antimicrobial susceptibility of lactic acid bacteria strains of potential use as feed additives — the basic safety and usefulness criterion. Frontiers in Veterinary Science, 8, Article 687071. https://doi.org/10.3389/fvets.2021.687071
39. Yilmaz, N., Ozogul, Y., Dağgeçen, E. C., Akyol, I., Rathod, N. B., Surasani, V. K. R. et al. (2025). Isolation, characterization and antibiotic resistance of lactic acid bacteria from dairy and seafood sources. Food Bioscience, 64, Article 105895. https://doi.org/10.1016/j.fbio.2025.105895
40. Hamdaoui, N., Benkirane, C., Bouaamali, H., Azghar, A., Mouncif, M., Maleb, A. et al. (2024). Investigating lactic acid bacteria genus Lactococcus lactis properties: Antioxidant activity, antibiotic resistance, and antibacterial activity against multidrug-resistant bacteria Staphylococcus aureus. Heliyon, 10(11), Article e31957. https://doi.org/10.1016/j.heliyon.2024.e31957
41. Floris, I., Battistini, R., Tramuta, C., Garcia-Vozmediano, A., Musolino, N., Scardino, G. et al. (2025). Antibiotic resistance in lactic acid bacteria fromdairy products in Northern Italy. Antibiotics, 14(4), Article 375. https://doi.org/10.3390/antibiotics14040375
42. Dec, M., Nowaczek, A., Stępień-Pyśniak, D., Wawrzykowski, J., Urban-Chmiel, R. (2018). Identification and antibiotic susceptibility of lactobacilli isolated from turkeys. BMC Microbiology, 18(1), Article 168. https://doi.org/10.1186/s12866-018-1269-6
43. Erginkaya, Z., Turhan, E. U., Tatlı, D. (2018). Determination of antibiotic resistance of lactic acid bacteria isolated from traditional Turkish fermented dairy products. Iranian Journal of Veterinary Research, 19(1), 53–56.
44. Dec, M., Stępień-Pyśniak, D., Nowaczek, A., Puchalski, A., Urban-Chmiel, R. (2020). Phenotypic and genotypic antimicrobial resistance profiles of fecal lactobacilli from domesticated pigeons in Poland. Anaerobe, 65, Article 102251. https://doi.org/10.1016/j.anaerobe.2020.102251
45. Duche, R. T., Singh, A., Wandhare, A. G., Sangwan, V., Sihag, M. K., Nwagu, T. N. et al. (2023). Antibiotic resistance in potential probiotic lactic acid bacteria of fermented foods and human origin from Nigeria. BMC Microbiology, 23(1), Article 142. https://doi.org/10.1186/s12866-023-02883-0
46. Obioha, P. I., Anyogu, A., Awamaria, B., Ghoddusi, H. B., Ouoba, L. I. I. (2023). Antimicrobial resistance of lactic acid bacteria from Nono, a naturally fermented milk product. Antibiotics, 12(5), Article 843. https://doi.org/10.3390/antibiotics12050843
47. Grujović, M. Ž., Marković, K. G., Morais, S., Semedo-Lemsaddek, T. (2024). Unveiling the potential of lactic acid bacteria from Serbian goat cheese. Foods, 13(13), Article 2065. https://doi.org/10.3390/foods13132065
48. Kiani, A., Nami, Y., Barghi, A., Salehian, M., Goudarzi, F., Haghshenas, B. (2025). Synergistic antimicrobial and probiotic activity of lactic acid bacteria isolated from Tarkhineh against Candida albicans. Scientific Reports, 15, Article 20651. https://doi.org/10.1038/s41598-025-07549-7
49. Anisimova, E., Gorokhova, I., Karimullina, G., Yarullina, D. (2022). Alarming antibiotic resistance of lactobacilli isolated from probiotic preparations and dietary supplements. Antibiotics, 11(11), Article 1557. https://doi.org/10.3390/antibiotics11111557
50. Nalepa, B., Markiewicz, L. H. (2022). Microbiological biodiversity of regional cow, goat and ewe milk cheeses produced in poland and antibiotic resistance of lactic acid bacteria isolated from them. Animals, 13(1), Article 168. https://doi.org/10.3390/ani13010168
51. Li, X., Li, W., Zhao, L., Li, Y., He, W., Ding, K., Cao, P. (2024). Characterization and assessment of native lactic acid bacteria from broiler intestines for potential probiotic properties. Microorganisms, 12(4), Article 749. https://doi.org/10.3390/microorganisms12040749
52. Reuben, R. C., Roy, P. C., Sarkar, S. L., Alam, R. U., Jahid, I. K. (2019). Isolation, characterization, and assessment of lactic acid bacteria toward their selection as poultry probiotics. BMC Microbiology, 19, Article 253. https://doi.org/10.1186/s12866-019-1626-0
53. Dowarah, R., Verma, A. K., Agarwal, N., Singh, P., Singh, B. R. (2018). Selection and characterization of probiotic lactic acid bacteria and its impact on growth, nutrient digestibility, health and antioxidant status in weaned piglets. PloS One, 13(3), Article e0192978. https://doi.org/10.1371/journal.pone.0192978
54. Escobar, G. D., Pelaggio, R., Cardozo, G., Moreno, S., De Torres, E., Rey, F. et al. (2023). Transfer of β-lactam and tetracycline antibiotics from spiked bovine milk to Dambo-type cheese, whey, and whey powder. Food Additives and Contaminants: Part A, 40(7), 824–837. https://doi.org/10.1080/19440049.2023.2220427
55. Fodor, A., Cseppento, D. C. N., Badea, G. E., Petrehele, A. I., Groze, A., Tit, D. M. et al. (2023). Colloidal gold immunochromatography and ELISA traceability of tetracycline residues from raw milk to its dairy products. In Vivo, 37(4), 1619–1627. https://doi.org/10.21873/invivo.13247
56. Lanyi, K., Darnay, L., Laszlo, N., Lehel, J., Friedrich, L., Győri, R. et al. (2021). Transfer of certain beta-lactam antibiotics from cow’s milk to fresh cheese and whey. Food Additives and Contaminants: Part A, 39(1), 52–60. https://doi.org/10.1080/19440049.2021.1973114
Review
For citations:
Sviridenko G.M., Zakharova M.B., Mamykin D.S. Risks of reducing safety of cheese-making products depending on the composition of antibiotics in milk. Food systems. 2026;9(2):199-207. (In Russ.) https://doi.org/10.21323/2618-9771-2026-9-2-199-207
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