Antimicrobial resistance of Salmonella spp. detected in animal products in 2022–2024
https://doi.org/10.29326/2304-196X-2025-14-3-310-318
Abstract
Introduction. Although antibiotics represent one of humanity’s greatest discoveries, their improper use can cause significant harm and lead to severe consequences. Objective. Testing of animal product samples followed by Salmonella spp. isolation, typing, identification and assessment of their antimicrobial resistance dynamics.
Materials and methods. The study was carried out at the Department for Microbiological Testing of the Vladimir Testing Laboratory of the Federal Centre for Animal Health. The disc diffusion test was used to determine bacteria resistance to antibiotics. The sizes of the microorganism growth inhibition zones were interpreted according to the Russian recommendations “Determination of the sensitivity of microorganisms to antimicrobial drugs” (IACMAC, version 2025-01), prepared on the basis of the European Committee on Antimicrobial Susceptibility Testing (EUCAST) recommendations and using CLSI M100 standard. PETSAL® monovalent and polyvalent O- and H-sera (The Saint Petersburg Scientific Research Institute ofVaccines and Serums of the FMBA of Russia) were used for serological identification. Antimicrobial resistance genes (blaCTX-M, blaOXA10, blaDHA, blaDES, blaKPC, blaOXA48-like, blaNDM, blaVIM) were identified by real-time polymerase chain reaction using the RESISTOM test systems (“LITECH”Co. Ltd., Russia).
Results. Forty-two Salmonella spp. isolates were recovered from animal product samples in 2022–2024. S. Enteritidis was the most frequently isolated serovar, and Salmonella spp. were predominantly isolated from poultry meat products. The detected isolates demonstrated maximum resistance to benzylpenicillin, erythromycin, norfloxacin, and tetracycline. Most of the isolates showed multiple resistance to several antimicrobials. Increased resistance to cephalosporins, fluoroquinolones, tetracyclines, aminoglycosides, chloramphenicol/levomycetin and sulfamethoxazole/trimethoprim was demonstrated for Salmonella spp. isolates. No antimicrobial resistance genes were detected when the isolates were tested with real-time polymerase chain reaction.
Conclusion. The study demonstrated widespread antimicrobial resistance, including multiple resistance, among Salmonella spp. isolates detected in animal products in 2022–2024.
Keywords
About the Authors
O. A. AkulichRussian Federation
Olga А. Akulich - Postgraduate Student, Federal Centre for Animal Health.
6 Gvardeyskaya str., Yur’evets, Vladimir 600901
N. B. Shadrova
Russian Federation
Natalya B. Shadrova - Cand. Sci. (Biology), Head of Department for Microbiological Testing, Federal Centre for Animal Health.
6 Gvardeyskaya str., Yur’evets, Vladimir 600901
G. S. Denisova
Russian Federation
Galina S. Denisova - Cand. Sci. (Biology), Head of the Vladimir Testing Centre, Federal Centre for Animal Health.
6 Gvardeyskaya str., Yur’evets, Vladimir 600901
References
1. WHO Bacterial Priority Pathogens List, 2024: bacterial pathogens of public health importance to guide research, development and strategies to prevent and control antimicrobial resistance. Geneva: World Health Organization; 2024. 56 р. https://iris.who.int/bitstream/handle/10665/376776/9789240093461-eng.pdf?sequence=1
2. World Health Organization.Ten threats to global health in 2019. https://www.who.int/news-room/spotlight/ten-threats-to-global-health-in-2019
3. World health statistics 2024: monitoring health for the SDGs, Sustainable Development Goals. Geneva: World Health Organization; 2024. 86 р. https://iris.who.int/bitstream/handle/10665/376869/9789240094703-eng.pdf
4. Tarín-Pelló A., Suay-García B., Pérez-Gracia M.-T. Antibiotic resistant bacteria: current situation and treatment options to accelerate the development of a new antimicrobial arsenal. Expert Review of Anti-Infective Therapy. 2022; 20 (8): 1095–1108. https://doi.org/10.1080/14787210.2022.2078308
5. Di K. N., Pham D. T., Tee T. S., Binh Q. A., Nguyen T. C. Antibiotic usage and resistance in animal production in Vietnam: a review of existing literature. Tropical Animal Health and Production. 2021; 53 (3):340. https://doi.org/10.1007/s11250-021-02780-6
6. Mukhina E., Artemieva M., Sakunts L., Tozhiboeva B. The social problem of antibiotic resistance. Universum: Medicine & Pharmacology. 2017; (6). https://7universum.com/ru/med/archive/item/4898 (in Russ.)
7. Manyi-Loh C., Mamphweli S., Meyer E., Okoh A. Antibiotic use in agriculture and its consequential resistance in environmental sources: potential public health implications. Molecules. 2018; 23 (4):795. https://doi.org/10.3390/molecules23040795
8. Aleksandrowicz A., Carolak E., Dutkiewicz A., Błachut A., Waszczuk W., Grzymajlo K. Better together – Salmonella biofilm-associated antibiotic resistance. Gut Microbes. 2023; 15 (1):2229937. https://doi.org/10.1080/19490976.2023.2229937
9. Wang B. X., Butler D. S. С., Hamblin M., Monack D. M. One species, different diseases: the unique molecular mechanisms that underlie the pathogenesis of typhoidal Salmonella infections. Current Opinion in Microbiology. 2023; 72:102262. https://doi.org/10.1016/j.mib.2022.102262
10. Li S., He Y., Mann D. A., Deng X. Global spread of Salmonella Enteritidis via centralized sourcing and international trade of poultry breeding stocks. Nature Communications. 2021; 12:5109. https://doi.org/10.1038/s41467-021-25319-7
11. Egorova S. A., Kaftyreva L. A., Pomazanov V. V. Current trends in the development of resistance to clinically significant antibiotics in Salmonella (review of literature). Russian Clinical LaboratoryDiagnostics. 2020; 65 (5): 308–315. http://dx.doi.org/10.18821/0869-2084-2020-65-5-308-315 (in Russ.)
12. World Animal Protection: Global public health cost of antimicrobial resistance related to antibiotic use on factory farms. https://www.world-animalprotection.org.in/globalassets/pdfs/reports/english/global-public-health-technical-report.pdf
13. WHO estimates of the global burden of foodborne diseases: food-borne disease burden epidemiology reference group 2007–2015. Geneva: World Health Organization; 2015. 254 p. https://iris.who.int/bitstream/handle/10665/199350/9789241565165_eng.pdf?sequence=1
14. Wu S., Hulme J. P. Recent advances in the detection of antibiotic and multi-drug resistant Salmonella: an update. International Journal of Molecular Sciences. 2021; 22 (7):3499. https://doi.org/10.3390/ijms22073499
15. Determination of the sensitivity of microorganisms to antimicrobial drugs: Russian recommendations. Version 2025-01. Smolensk: Smolensk State Medical University; Interregional Association for Clinical Microbiology and Antimicrobial Chemotherapy; 2025. 208 р. https://www.antibiotic.ru/library/ocmap2025 (in Russ.)
16. European Committee on Antimicrobial Susceptibility Testing. Routine and extended internal quality control for MIC determination and disk diffusion as recommended by EUCAST. Version 15.0, valid from 2025-01-01. https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/QC/v_15.0_EUCAST_QC_tables_routine_and_extended_QC.pdf
17. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing. 35th ed. CLSI supplement M100. Clinical and Laboratory Standards Institute; 2025. 428 p.
18. Salmonellosis. In: European Centre for Disease Prevention and Control. Annual Epidemiological Report for 2022. Stockholm: ECDC; 2024. https://www.ecdc.europa.eu/en/publications-data/salmonellosis-annual-epidemiological-report-2022
19. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2022–2023. EFSA Journal. 2025; 23 (3):e9237. https://doi.org/10.2903/j.efsa.2025.9237
20. Vitkova O. N., Belousov V. I., Ivanova O. E., Bazarbaev S. B. Study of antibiotic resistance of Salmonella isolates from animals and fodders of animal origin on the territory of the Russian Federation. Veterinaria Kubani. 2015; (2): 11–15. https://elibrary.ru/tppjdx (in Russ.)
21. Rakitin A. L., Yushina Y. K, Zaiko E. V., Bataeva D. S., Kuznetsova O. A., Semenova A. A., et al. Evaluation of antibiotic resistance of Salmonella serotypes and whole-genome sequencing of multiresistant strains isolated from food products in Russia. Antibiotics. 2022; 11 (1):1. https://doi.org/10.3390/antibiotics11010001
22. Mendybaeva A. M., Ruzauskas M., Aleshina Yu. E., Alieva G. K., Mukanov G. B., Ryshchanova R. M. Opportunistic and pathogenic microflora antibiotics resistance risk assessment extracted from animal products. Bulletin KrasSAU. 2022; (2): 147–156. https://doi.org/10.36718/1819-4036-2022-2-147-156 (in Russ.)
23. Patchanee P., Tansiricharoenkul K., Buawiratlert T., Wiratsudakul A., Angchokchatchawal K., Yamsakul P., et al. Salmonella in pork retail outlets and dissemination of its pulsotypes through pig production chain in Chiang Mai and surrounding areas, Thailand. Preventive Veterinary Medicine. 2016; 130: 99–105. https://doi.org/10.1016/j.prevetmed.2016.06.013
24. Possebon F. S., Tiba Casas M. R., Nero L. A., Yamatogi R. S., Araújo J. P. Jr., Pinto J. P. A. N. Prevalence, antibiotic resistance, PFGE and MLST characterization of Salmonella in swine mesenteric lymph nodes. Preventive Veterinary Medicine. 2020; 179:105024. https://doi.org/10.1016/j.prevetmed.2020.105024
25. Solov’yeva A. S., Shubin F. N., Kuznetsova N. A. Antibiotic resistance of Salmonella enteritidis sticks allocated in the Far Eastern and Siberian Federal Districts. Health. Medical ecology. Science. 2017; (5): 15–21. https://doi.org/10.5281/zenodo.1115444 (in Russ.)
26. Baquero F. Threats of antibiotic resistance: an obliged reappraisal. International Microbiology. 2021; 24 (4): 499–506. https://doi.org/10.1007/s10123-021-00184-y
27. Wen S. C. H., Best E., Nourse C. Non-typhoidal Salmonella infections in children: review of literature and recommendations for management. Journal of Paediatrics and Child Health. 2017; 53 (10): 936–941. https://doi.org/10.1111/jpc.13585
28. Konyali D., Guzel M., SoyerY. Genomic characterization of Salmonella enterica resistant to cephalosporin, quinolones, and macrolides. Current Microbiology. 2023; 80 (11):344. https://doi.org/10.1007/s00284-023-03458-y
Review
For citations:
Akulich O.A., Shadrova N.B., Denisova G.S. Antimicrobial resistance of Salmonella spp. detected in animal products in 2022–2024. Veterinary Science Today. 2025;14(3):310-318. (In Russ.) https://doi.org/10.29326/2304-196X-2025-14-3-310-318