Resistance profile to antimicrobial agents of Staphylococcus aureus and Enterococcus faecalis isolated in the Kyrgyz Republic
- Authors: Koroleva I.B.1, Kulikova N.G.1, Bityumina L.A.1, Mikhailova Y.V.1, Shelenkov A.A.1, Karpenko A.E.1, Kondrateva D.K.1, Amankulova G.E.2, Dzhumakanova A.B.2, Manzeniuk I.N.1, Akimkin V.G.1
-
Affiliations:
- Central Research Institute of Epidemiology
- Department of Disease Prevention and State Sanitary and Epidemiological Surveillance
- Pages: 23-34
- Section: Original study articles
- Submitted: 17.02.2025
- Accepted: 11.04.2025
- Published: 15.07.2025
- URL: https://rjeid.com/1560-9529/article/view/655873
- DOI: https://doi.org/10.17816/EID655873
- EDN: https://elibrary.ru/TYDPBX
- ID: 655873
Cite item
Abstract
BACKGROUND: The dissemination of antibacterial-resistant microorganisms and resistance genes via food products represents a significant threat to global public health.
AIM: The study aimed to conduct epidemiological monitoring of antibiotic-resistant bacteria isolated from food products in the Kyrgyz Republic through the study of their phenotypic and genotypic susceptibility profiles.
METHODS: It was a cross-sectional observational study. Microorganism species identification was performed using MALDI-TOF mass spectrometry. Phenotypic susceptibility to 35 antimicrobial agents was assessed by minimum inhibitory concentration testing. Genes conferring resistance to antimicrobial agents were detected by whole-genome sequencing.
RESULTS: The study subjects were antibiotic-resistant strains of Staphylococcus aureus (n = 16) and Enterococcus faecalis (n = 36) isolated from ready-to-eat food products in the Kyrgyz Republic between 2020 and 2023. The findings indicate a predominance of antibiotic-resistant strains in dairy and meat products as well as in water. The isolates of each species were found to belong to 3 sequence types: S. aureus (ST5, ST15, ST45); E. faecalis (ST21, ST133, ST179). According to the obtained data, all S. aureus isolates carrying the β-lactam resistance gene blaZ were phenotypically resistant to this class of antibiotics. Despite phenotypic resistance to vancomycin, linezolid, and daptomycin observed in 25% of S. aureus isolates, no genetic markers of resistance to these reserve antibiotics were identified. E. faecalis isolates carrying the tetM gene were phenotypically resistant to tetracycline, with the overall proportion of tetracycline-resistant strains reaching 83.3%. A high proportion of E. faecalis carrying the macrolide resistance gene lsaA, accounting for 31.7%, corresponds to the data on the expected phenotypic resistance of this microorganism.
CONCLUSION: The studies conducted in the Kyrgyz Republic confirm the need for monitoring the spread of antimicrobial resistance in pathogens through the food chain.
Full Text

About the authors
Irina B. Koroleva
Central Research Institute of Epidemiology
Author for correspondence.
Email: martiusheva@cmd.su
ORCID iD: 0000-0002-9397-9646
SPIN-code: 5463-6656
Russian Federation, 3A Novogireevskay st, Moscow, 111123
Nina G. Kulikova
Central Research Institute of Epidemiology
Email: kulikova_ng@cmd.su
ORCID iD: 0000-0002-1716-6969
SPIN-code: 8876-0698
Cand. Sci. (Biology)
Russian Federation, MoscowLyutsiya A. Bityumina
Central Research Institute of Epidemiology
Email: bitumina@cmd.su
ORCID iD: 0000-0002-5378-0827
SPIN-code: 2311-2279
Russian Federation, Moscow
Yulia V. Mikhailova
Central Research Institute of Epidemiology
Email: mihailova@cmd.su
ORCID iD: 0000-0002-5646-538X
SPIN-code: 4271-1072
Cand. Sci. (Biology)
Russian Federation, MoscowAndrey A. Shelenkov
Central Research Institute of Epidemiology
Email: shelenkov@cmd.su
ORCID iD: 0000-0002-7409-077X
SPIN-code: 6710-7264
Cand. Sci. (Physics and Mathematics)
Russian Federation, MoscowAnna E. Karpenko
Central Research Institute of Epidemiology
Email: a.egorova@cmd.su
ORCID iD: 0000-0003-0486-1353
SPIN-code: 6350-1373
Russian Federation, Moscow
Daria K. Kondrateva
Central Research Institute of Epidemiology
Email: kondrateva@cmd.su
ORCID iD: 0009-0009-6693-3990
SPIN-code: 4634-9319
Russian Federation, Moscow
Gulnara E. Amankulova
Department of Disease Prevention and State Sanitary and Epidemiological Surveillance
Email: amankulova_63@mail.ru
ORCID iD: 0009-0000-0256-3913
Kyrgyzstan, Bishkek
Aigul B. Dzhumakanova
Department of Disease Prevention and State Sanitary and Epidemiological Surveillance
Email: aigul.dzumakanova.dgsn@mail.ru
ORCID iD: 0009-0005-9065-6744
Kyrgyzstan, Bishkek
Igor N. Manzeniuk
Central Research Institute of Epidemiology
Email: manzeniuk@cmd.su
ORCID iD: 0000-0002-1146-1430
SPIN-code: 5013-6441
MD, Cand. Sci. (Medicine)
Russian Federation, MoscowVasiliy G. Akimkin
Central Research Institute of Epidemiology
Email: vgakimkin@yandex.ru
ORCID iD: 0000-0003-4228-9044
SPIN-code: 4038-7455
MD, Dr. Sci. (Medicine), Professor, academician of the Russian Academy of Sciences
Russian Federation, MoscowReferences
- World Health Organization. WHO Bacterial Priority Pathogenes List, 2024: Bacterial Pathogens of Public Health Importance to Guide Research, Development and Strategies to Prevent and Control Antimicrobial Resistance [Internet]. Geneva: World Health Organization; 2024 [cited 2024 Jul 21]. ISBN: 978-92-4-009346-1 Available from: https://iris.who.int/bitstream/handle/10665/376776/9789240093461-eng.pdf
- Govindaraj Vaithinathan A, Vanitha A. WHO Global Priority Pathogens List on Antibiotic Resistance: An Urgent Need for Action to Integrate One Health Data. Perspect Public Health. 2018;138(2):87–88. doi: 10.1177/1757913917743881
- European Food Safety Authority, European Centre for Disease Prevention and Control. The European Union One Health 2022 Zoonoses Report. EFSA Journal. 2023;21(12):e8442. doi: 10.2903/j.efsa.2023.8442
- Spoor LE, McAdam PR, Weinert LA, et al. Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant Staphylococcus aureus. mBio. 2013;4(4). doi: 10.1128/mBio.00356-13 EDN: YEFPFB
- Chen H, Zhang J, He Y, et al. Exploring the Role of Staphylococcus aureus in Inflammatory Diseases. Toxins. 2022;14(7):464. doi: 10.3390/toxins14070464 EDN: KRTLSL
- Golob M, Pate M, Kušar D, et al. Antimicrobial Resistance and Virulence Genes in Enterococcus faecium and Enterococcus faecalis from Humans and Retail Red Meat. Biomed Res Int. 2019;2019:2815279. doi: 10.1155/2019/2815279
- Dendani Chadi Z, Dib L, Zeroual F, Benakhla A. Usefulness of Molecular Typing Methods for Epidemiological and Evolutionary Studies of Staphylococcus aureus Isolated From Bovine Intramammary Infections. Saudi Journal of Biological Sciences. 2022;29(8):103338. doi: 10.1016/j.sjbs.2022.103338 EDN: ZCFXNY
- Dendani Chadi Z, Arcangioli MA. Pulsed-Field Gel Electrophoresis Analysis of Bovine Associated Staphylococcus aureus: A Review. Pathogens. 2023;12(7):966. doi: 10.3390/pathogens12070966 EDN: PERGQD
- Strommenger B, Layer F, Werner G. Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus in Workers in the Food Industry. In: Fetsch A. Staphylococcus aureus. Academic Press; 2018. P. 163–188. ISBN: 978-0-12-809671-0 doi: 10.1016/B978-0-12-809671-0.00009-7
- Fiore E, Van Tyne D, Gilmore MS. Pathogenicity of Enterococci. Microbiology Spectrum. 2019;7(4). doi: 10.1128/microbiolspec.GPP3-0053-2018
- Jolley KA, Bray JE, Maiden MCJ. Open-access Bacterial Population Genomics: BIGSdb Software, the PubMLST.org Website and Their Applications. Wellcome Open Research. 2018;3:124. doi: 10.12688/wellcomeopenres.14826.1
- Bankevich A, Nurk S, Antipov D, et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. Journal of Computational Biology. 2012;19(5):455–477. doi: 10.1089/cmb.2012.0021 EDN: PDOPXT
- Shelenkov A, Mikhaylova Y, Yanushevich Y, et al. Molecular Typing, Characterization of Antimicrobial Resistance, Virulence Profiling and Analysis of Whole-Genome Sequence of Clinical Klebsiella pneumoniae Isolates. Antibiotics. 2020;9(5):261. doi: 10.3390/antibiotics9050261 EDN: MVCPAP
- Murlenkov NV. Problems and Factors of Development of Antibiotic Resistance in Agriculture. Biologija v sel’skom hozjajstve. 2019;(4):11–14. EDN: JNLYWI
- Mak PHW, Rehman MA, Kiarie EG, et al. Production Systems and Important Antimicrobial Resistant-Pathogenic Bacteria in Poultry: A Review. Journal of Animal Science and Biotechnology. 2022;13(1):1–20. doi: 10.1186/s40104-022-00786-0 EDN: IVPZXZ
- Kuzminsky II, Stepanova EA, Zhashko NV, Radyush IS. Resistance of Microorganisms Isolated From Endometritis in Cows to the Antimicrobial Drugs Used. In: Proceedings of the International Scientific and Practical Conference dedicated to the 95th anniversary of the Department of Obstetrics, Gynecology and Biotechnology of Animal Reproduction and the 45th anniversary of the veterinary and scientific and practical activities of Professor R.G. Kuzmich “Problems of Animal Reproductive Health and Ways to Solve Them”. Vitebsk: Vitebsk State Akademy or Veterinary Medicine; 2022. P. 48–51. EDN: PLYZDK
- Mekhloufi OA, Chieffi D, Hammoudi A, et al. Prevalence, Enterotoxigenic Potential and Antimicrobial Resistance of Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus (MRSA) Isolated from Algerian Ready to Eat Foods. Toxins. 2021;13(12):835. doi: 10.3390/toxins13120835 EDN: WQWNDT
- Kulikova NG, Chernyshkov AV, Mikhaylova YV, et al. Antimicrobial Resistance of Staphylococcus aureus Isolates Isolated From Food Products in the Territory of the Republic of Kazakhstan. Infectious Diseases. 2024;22(1):91–99. doi: 10.20953/1729-9225-2024-1-91-99 EDN: MJETCL
- Kayumova MU, Ruziev MM, Kulikova NG, et al. Antibiotic Resistance of Foodborne Microorganisms Isolated in the Republic of Tajikistan. Public Health and Life Environment — PH&LE. 2024;32(4):45–50. doi: 10.35627/2219-5238/2023-32-4-45-50 EDN: ROFEEI
- Hanson BM, Dressler AE, Harper AL, et al. Prevalence of Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus (MRSA) on Retail Meat in Iowa. Journal of Infection and Public Health. 2011;4(4):169–174. doi: 10.1016/j.jiph.2011.06.001
- Abdalrahman L, Wells H, Fakhr M. Staphylococcus aureus is More Prevalent in Retail Beef Livers than in Pork and other Beef Cuts. Pathogens. 2015;4(2):182–198. doi: 10.3390/pathogens4020182
- Thwala T, Madoroba E, Basson A, Butaye P. Prevalence and Characteristics of Staphylococcus aureus Associated with Meat and Meat Products in African Countries: A Review. Antibiotics. 2021;10(9):1108. doi: 10.3390/antibiotics10091108 EDN: CKZCYE
- Wu S, Huang J, Wu Q, et al. Staphylococcus aureus Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity. Frontiers in Microbiology. 2018;9:2767. doi: 10.3389/fmicb.2018.02767
- Lv G, Jiang R, Zhang H, et al. Molecular Characteristics of Staphylococcus aureus From Food Samples and Food Poisoning Outbreaks in Shijiazhuang, China. Frontiers in Microbiology. 2021;12:652276. doi: 10.3389/fmicb.2021.652276 EDN: GNVMOC
- Ning K, Zhou R, Li M. Antimicrobial Resistance and Molecular Typing of Staphylococcus aureus Isolates From Raw Milk in Hunan Province. PeerJ. 2023;11:e15847. doi: 10.7717/peerj.15847 EDN: SLTENO
- Katayama Y, Zhang HZ, Hong D, Chambers HF. Jumping the Barrier to Beta-Lactam Resistance in Staphylococcus aureus. J Bacteriol. 2003;185(18):5465–5472. doi: 10.1128/JB.185.18.5465-5472.2003
- Guo YH, He ZL, Ji QL, et al.. Population Structure of Food-Borne Staphylococcus aureus in China. Zhonghua Liu Xing Bing Xue Za Zhi. 2023;44(6):982–989. doi: 10.3760/cma.j.cn112338-20221206-01043
- Sadat A, Shata RR, Farag AMM, et al. Prevalence and Characterization of PVL-Positive Staphylococcus aureus Isolated from Raw Cow’s Milk. Toxins. 2022;14(2):97. doi: 10.3390/toxins14020097 EDN: ESJZTN
- Beier R, Andrews K, Hume M, et al. Disinfectant and Antimicrobial Susceptibility Studies of Staphylococcus aureus Strains and ST398-MRSA and ST5-MRSA Strains from Swine Mandibular Lymph Node Tissue, Commercial Pork Sausage Meat and Swine Feces. Microorganisms. 2021;9(11):2401. doi: 10.3390/microorganisms9112401 EDN: RCYSHF
- Park S, Ronholm J. Staphylococcus aureus in Agriculture: Lessons in Evolution from a Multispecies Pathogen. Clinical Microbiology Reviews. 2021;34(2). doi: 10.1128/cmr.00182-20 EDN: WFZAFI
- Pérez-Boto D, D’Arrigo M, García-Lafuente A, et al. Staphylococcus aureus in the Processing Environment of Cured Meat Products. Foods. 2023;12(11):2161. doi: 10.3390/foods12112161 EDN: KXNQQA
- Naorem RS, Goswami G, Gyorgy S, Fekete C. Comparative analysis of prophages carried by human and animal-associated Staphylococcus aureus strains spreading across the European regions. Scientific Reports. 2021;11(1):18994. doi: 10.1038/s41598-021-98432-8 EDN: WWZMQX
- Wang H, Shen J, Zhu C, et al. Antibiotics Resistance and Virulence of Staphylococcus aureus Isolates Isolated from Raw Milk from Handmade Dairy Retail Stores in Hefei City, China. Foods. 2022;11(15):2185. doi: 10.3390/foods11152185 EDN: MTESAK
- Zhu Z, Liu X, Chen X, et al. Prevalence and Virulence Determinants of Staphylococcus aureus in Wholesale and Retail Pork in Wuhan, Central China. Foods. 2022;11(24):4114. doi: 10.3390/foods11244114 EDN: FFTZDT
- Lowder BV, Guinane CM, Ben Zakour NL, et al. Recent Human-to-poultry Host Jump, Adaptation, and Pandemic Spread of Staphylococcus aureus. Proceedings of the National Academy of Sciences. 2009;106(46):19545–19550. doi: 10.1073/pnas.0909285106
- El-Telbany M, Lin CY, Abdelaziz MN, et al. Potential Application of Phage vB_EfKS5 to control Enterococcus faecalis and its Biofilm in Food. AMB Express. 2023;13(1):130. doi: 10.1186/s13568-023-01628-6 EDN: ANWUCB
- Holman DB, Klima CL, Gzyl KE, et al. Antimicrobial Resistance in Enterococcus spp. Isolated from a Beef Processing Plant and Retail Ground Beef. Microbiology Spectrum. 2021;9(3):e01980-21. doi: 10.1128/Spectrum.01980-21 EDN: GYEAGX
- Wei L, Wu Q, Zhang J, et al. Prevalence and Genetic Diversity of Enterococcus faecalis Isolates from Mineral Water and Spring Water in China. Frontiers in Microbiology. 2017;8:1109. doi: 10.3389/fmicb.2017.01109
- Cho S, Jackson CR, Frye JG. The prevalence and antimicrobial resistance phenotypes of Salmonella, Escherichia coli and Enterococcus sp. in surface water. Letters in Applied Microbiology. 2020;71(1):3–25. doi: 10.1111/lam.13301 EDN: TLEFBM
- The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters [Internet]. Version 13.0. В: The European Committee on Antimicrobial Susceptibility Testing, 2023–2024. Available from: http://www.eucast.org
- Gołaś-Prądzyńska M, Łuszczyńska M, Rola JG. Dairy Products: A Potential Source of Multidrug-Resistant Enterococcus faecalis and Enterococcus faecium Strains. Foods. 2022;11(24):4116. doi: 10.3390/foods11244116 EDN: ZGUZIG
- Li J, Yang L, Huang X, et al. Molecular Characterization of Antimicrobial Resistance and Virulence Factors of Enterococcus faecalis from Ducks at Slaughterhouses. Poultry Science. 2022;101(4):101646. doi: 10.1016/j.psj.2021.101646 EDN: OJEFLQ
- EFSA Panel on Animal Health and Welfare, More S, Bicout D, et al. Assessment of Listing and Categorisation of Animal Diseases Within the Framework of the Animal Health Law (Regulation (EU) No. 2016/429): Bluetongue. EFSA Journal. 2017;15(8):e04957. doi: 10.2903/j.efsa.2017.4957
- Kim E, Shin SW, Kwak HS, et al. Prevalence and Characteristics of Phenicol-Oxazolidinone Resistance Genes in Enterococcus Faecalis and Enterococcus Faecium Isolated from Food-Producing Animals and Meat in Korea. International Journal of Molecular Sciences. 2021;22(21):11335. doi: 10.3390/ijms222111335 EDN: EUVWJM
- Zheng JX, Wu Y, Lin ZW, et al. Characteristics of and Virulence Factors Associated with Biofilm Formation in Clinical Enterococcus faecalis Isolates in China. Frontiers in Microbiology. 2017;8:272233. doi: 10.3389/fmicb.2017.02338
- Farias BO, Montenegro KS, Nascimento APA, et al. First Report of a Wastewater Treatment-Adapted Enterococcus faecalis ST21 Harboring vanA Gene in Brazil. Current Microbiology. 2023;80(9):313. doi: 10.1007/s00284-023-03418-6 EDN: WUTCXH
- Neumann B, Prior K, Bender JK, et al. A Core Genome Multilocus Sequence Typing Scheme for Enterococcus faecalis. Journal of Clinical Microbiology. 2019;57(3):e01686-18. doi: 10.1128/JCM.01686-18 EDN: MKTCCC
- Pöntinen AK, Top J, Arredondo-Alonso S, et al. Apparent Nosocomial Adaptation of Enterococcus faecalis Predates the Modern Hospital Era. Nat Commun. 2021;12(1):1523. doi: 10.1038/s41467-021-21749-5
- Zaitseva EA, Luchaninova VN, Melnikova EA, et al. Clinical and Microbiological Aspects of Enterococcus faecalis-associated Urinary Tract Infection. Russian Journal of Infection and Immunity. 2021;11(1):184–190. doi: 10.15789/2220-7619-CAM-1341 EDN: XIZSPD
- Moles L, Gómez M, Jiménez E, et al. Preterm Infant Gut Colonization in the Neonatal ICU and Complete Restoration 2 years later. Clinical Microbiology and Infection. 2015;21(10):936.e1–936.e10. doi: 10.1016/j.cmi.2015.06.003
- Biggel M, Nüesch-Inderbinen M, Raschle S, et al. Spread of Vancomycin-Resistant Enterococcus faecium ST133 in the Aquatic Environment in Switzerland. Journal of Global Antimicrobial Resistance. 2021;27:31–36. doi: 10.1016/j.jgar.2021.08.002 EDN: WLETUB
Supplementary files
