Antimicrobial resistance profile of Staphylococcus aureus and Enterococcus faecalis isolated in the Kyrgyz Republic



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Abstract

BACKGROUND: The dissemination of antibiotic-resistant microorganisms and resistance genes through food products is a serious problem for global public health. In this context, the aim of this study was to conduct surveillance of antibiotic-resistant bacteria isolated from food products in the Kyrgyz Republic by studying their phenotypic and genotypic susceptibility profiles.

AIM: Conducting epidemiological monitoring of antibiotic-resistant bacteria isolated from food products in the Kyrgyz Republic by analyzing their phenotypic and genotypic susceptibility profiles.

METHODS: The objects of the study were antibiotic-resistant bacterial cultures of S.aureus (n=16) and E.faecalis (n=36), isolated from ready-to-eat food products in the Kyrgyz Republic in the period 2020-2023. Identification of microorganisms was carried out using the MALDI-TOF method mass spectrometry. Phenotypic susceptibility was determined in relation to 20 antimicrobial drugs using the minimum inhibitory concentration method. Antimicrobial resistance genes were determined using data analysis of whole-genome sequencing.

RESULTS: The phenotypic profile and genetic markers of antibiotic resistance of foodborne microorganisms isolated in the Kyrgyz Republic were carried out for the first time. The studies indicate the prevalence of antibiotic-resistant strains in meat and dairy products and water. Each species under investigation belonged to 3 sequences-types: S.aureus (ST5, ST15, ST45), E.faecalis (ST21, ST133, ST179). According to the data obtained, all S.aureus carrying blaZ gene were phenotypically resistant to this group of antibiotics. S. aureus isolates resistant to vancomycin, linezolid and daptomycin did not have genetic determinants of resistance to these antimicrobial agents of last reserve. E.faecalis isolates carrying the tetM gene were phenotypically resistant to tetracycline, with the total number of resistant strains up to 83.3%. The presence of macrolide resistance gene lsaA in E.faecalis investigated is in a good accordance with the expected resistance phenotype of this microorganism.

CONCLUSION: Studies conducted in the Kyrgyz Republic confirm the need to monitor the spread of AMR pathogens through the food chain.

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About the authors

Irina B. Koroleva

FBIS Central Research Institute of Epidemiology of Rospotrebnadzor, Moscow, Russia

Author for correspondence.
Email: martiusheva@cmd.su
ORCID iD: 0000-0002-9397-9646
SPIN-code: 5463-6656
ResearcherId: LJL-0031-2024

junior researcher of Science group of Antimicrobial resistance of food pathogens

Russian Federation, 111123, Russia, Moscow, Novogireevskay st. 3A

Nina G. Kulikova

FBIS Central Research Institute of Epidemiology of Rospotrebnadzor, Moscow, Russia

Email: kulikova_ng@cmd.su
ORCID iD: 0000-0002-1716-6969
SPIN-code: 8876-0698

PhD (Biol.), senior Researcher of Science group of Antimicrobial resistance of food pathogens

Russian Federation, 111123, Russia, Moscow, Novogireevskay st. 3A

Lyutsiya A. Bitumina

FBIS Central Research Institute of Epidemiology of Rospotrebnadzor, Moscow, Russia

Email: bitumina@cmd.su
ORCID iD: 0000-0002-5378-0827
SPIN-code: 2311-2279
Russian Federation, 111123, Russia, Moscow, Novogireevskay st. 3A

Yulia V. Mikhailova

FBIS Central Research Institute of Epidemiology of Rospotrebnadzor, Moscow, Russia

Email: mihailova@cmd.su
ORCID iD: 0000-0002-5646-538X
SPIN-code: 4271-1072

Ph.D. in Biology, Head of the Laboratory of Molecular Mechanisms of Antibiotic Resistance

Russian Federation, 111123, Russia, Moscow, Novogireevskay st. 3A

Andrey A. Shelenkov

FBIS Central Research Institute of Epidemiology of Rospotrebnadzor, Moscow, Russia

Email: shelenkov@cmd.su
ORCID iD: 0000-0002-7409-077X
SPIN-code: 6710-7264

PhD (Appl.Math.), senior Researcher of Laboratory of Molecular Mechanisms of Antibiotic Resistance

Russian Federation, 111123, Russia, Moscow, Novogireevskay st. 3A

Anna E. Karpenko

FBIS Central Research Institute of Epidemiology of Rospotrebnadzor, Moscow, Russia

Email: a.egorova@cmd.su
ORCID iD: 0000-0003-0486-1353
SPIN-code: 6350-1373

Researcher of Laboratory of Molecular Mechanisms of Antibiotic Resistance

111123, Russia, Moscow, Novogireevskay st. 3A

Darya K. Kondratieva

FBIS Central Research Institute of Epidemiology of Rospotrebnadzor, Moscow, Russia

Email: kondrateva@cmd.su
ORCID iD: 0009-0009-6693-3990
SPIN-code: 4634-9319

junior researcher Laboratory of molecular mechanisms of antibiotic resistance

Russian Federation, 111123, Russia, Moscow, Novogireevskay st. 3A

G. E. Amankulova

Department of Disease Prevention and State Sanitary and Epidemiological Surveillance of the Ministry of Health of the Kyrgyz Republic, Bishkek, Kyrgyzstan

Email: amankulova_63@mail.ru

Head of the Reference Laboratory for Antimicrobial Resistance

Kyrgyzstan

A. B. Dzhumakanova

Department of Disease Prevention and State Sanitary and Epidemiological Surveillance of the Ministry of Health of the Kyrgyz Republic, Bishkek, Kyrgyzstan

Email: aigul.dzumakanova.dgsn@mail.ru
ORCID iD: 0009-0005-9065-6744

Head of the Laboratory Testing Center

Kyrgyzstan

Igor N. Manzeniuk

FBIS Central Research Institute of Epidemiology of Rospotrebnadzor, Moscow, Russia

Email: manzeniuk@cmd.su
ORCID iD: 0000-0002-1146-1430
SPIN-code: 5013-6441

PhD (Med.), assistant director for research

Russian Federation, 111123, Russia, Moscow, Novogireevskay st. 3A

Vasiliy G. Akimkin

FBIS Central Research Institute of Epidemiology of Rospotrebnadzor, Moscow, Russia

Email: vgakimkin@yandex.ru
ORCID iD: 0000-0003-4228-9044
SPIN-code: 4038-7455

Professor, Academician of the Russian Academy of Sciences, MD, Director

Russian Federation, 111123, Russia, Moscow, Novogireevskay st. 3A

References

  1. List W. H. O. B. P. P. Bacterial Pathogens of Public Health Importance to Guide Research, Development and Strategies to Prevent and Control Antimicrobial Resistance //World Health Organization: Geneva, Switzerland. – 2024;
  2. Asokan G. V., Vanitha A. WHO global priority pathogens list on antibiotic resistance: an urgent need for action to integrate One Health data //Perspectives in public health. – 2018. – Т. 138. – №. 2. – С. 87-88;
  3. Authority E. F. S. et al. The European Union One Health 2022 Zoonoses Report //EFSA Journal. – 2023. – Т. 21. – №. 12;
  4. Spoor L. E. et al. Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus //MBio. – 2013. – Т. 4. – №. 4. – С. 10.1128/mbio. 00356-13. doi: 10.1128/mBio.00356-13;
  5. Chen H. et al. Exploring the role of Staphylococcus aureus in inflammatory diseases //Toxins. – 2022. – Т. 14. – №. 7. – С. 464. doi: 10.3390/toxins14070464;
  6. SanPiN 2.1.4.1074-01 “Drinking water. Hygienic requirements for water quality of centralized drinking water supply systems. Quality control”;
  7. SanPiN 2.1.4.1116-02 “Drinking water. Hygienic requirements for the quality of water packaged in containers. Quality control”;Golob M. et al. Antimicrobial resistance and virulence genes in Enterococcus faecium and Enterococcus faecalis from humans and retail red meat //BioMed research international. – 2019. – Т. 2019. – №. 1. – С. 2815279. doi: 10.1155/2019/2815279;
  8. Chadi Z. D. et al. Usefulness of molecular typing methods for epidemiological and evolutionary studies of Staphylococcus aureus isolated from bovine intramammary infections //Saudi Journal of Biological Sciences. – 2022. – Т. 29. – №. 8. – С. 103338. doi: 10.1016/j.sjbs.2022.103338;
  9. Dendani Chadi Z., Arcangioli M. A. Pulsed-Field Gel Electrophoresis Analysis of Bovine Associated Staphylococcus aureus: A Review //Pathogens. – 2023. – Т. 12. – №. 7. – С. 966. doi: 10.3390/pathogens12070966;
  10. Strommenger B., Layer F., Werner G. Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in workers in the food industry //Staphylococcus aureus. – Academic Press, 2018. – С. 163-188. doi: 10.1016/B978-0-12-809671-0.00009-7;
  11. Fiore E., Van Tyne D., Gilmore M. S. Pathogenicity of enterococci //Microbiology spectrum. – 2019. – Т. 7. – №. 4. – С. 10.1128/microbiolspec. gpp3-0053-2018;
  12. Jolley K. A., Bray J. E., Maiden M. C. J. Open-access bacterial population genomics: BIGSdb software, the PubMLST. org website and their applications //Wellcome open research. – 2018. – Т. 3. doi: 10.12688/wellcomeopenres.14826.1;
  13. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012, 19, 455-477. doi: 10.1089/cmb.2012.0021;
  14. Shelenkov A et al. Molecular Typing, Characterization of Antimicrobial Resistance, Virulence Profiling and Analysis of Whole-Genome Sequence of Clinical Klebsiella pneumoniae Isolates. Antibiotics (Basel). 2020 May 17;9(5):261. doi: 10.3390/antibiotics9050261. PMID: 32429555; PMCID: PMC7277670;
  15. Murlenkov N. V. Problems and factors of antibiotic resistance development in agriculture //Biology in Agriculture. - 2019. - №. 4 (25). - С. 11-14;
  16. Mak P. H. W. et al. Production systems and important antimicrobial resistant-pathogenic bacteria in poultry: a review //Journal of Animal Science and Biotechnology. - 2022. - Т. 13. - №. 1. - P. 148. doi: 10.1186/s40104-022-00786-0;
  17. Kuzminsky I. I. et al. Resistance of microorganisms isolated in endometritis in cows to used antimicrobials. - 2022;
  18. Mekhloufi O. 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. - Т. 13. - №. 12. - С. 835. doi: 10.3390/toxins13120835;
  19. Kulikova N.G. et al. Resistance to antimicrobials isolates of Staphylococcus aureus isolated from food products in the territory of the Republic of Kazakhstan. //Infectious Diseases. - 2024 - Т.22, №1. - С. 91-99. doi: 10.20953/1729-9225-2024-1-91-99;
  20. Kayumova M. U. et al. Antibiotic resistance of microorganisms of food origin isolated on the territory of the Republic of Tajikistan // Public Health and Habitat-ZNiSO. - 2024. - Т. 32. - №. 4. - С. 45-50;Hanson B. M. et al. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa //Journal of infection and public health. – 2011. – Т. 4. – №. 4. – С. 169-174. https://doi.org/10.1016/j.jiph.2011.06.001;
  21. Abdalrahman L. S., Wells H., Fakhr M. K. Staphylococcus aureus is more prevalent in retail beef livers than in pork and other beef cuts //Pathogens. – 2015. – Т. 4. – №. 2. – С. 182-198. doi: 10.3390/pathogens4020182;
  22. Thwala T. et al. Prevalence and characteristics of Staphylococcus aureus associated with meat and meat products in African countries: a review //Antibiotics. – 2021. – Т. 10. – №. 9. – С. 1108. doi: 10.3390/antibiotics10091108;
  23. Wu S. et al. Staphylococcus aureus isolated from retail meat and meat products in China: incidence, antibiotic resistance and genetic diversity //Frontiers in microbiology. – 2018. – Т. 9. – С. 2767. doi: 10.3389/fmicb.2018.02767;
  24. Lv G. et al. Molecular characteristics of Staphylococcus aureus from food samples and food poisoning outbreaks in Shijiazhuang, China //Frontiers in Microbiology. – 2021. – Т. 12. – С. 652276. doi: 10.3389/fmicb.2021.652276;
  25. Ning K., Zhou R., Li M. Antimicrobial resistance and molecular typing of Staphylococcus aureus isolates from raw milk in Hunan Province //PeerJ. – 2023. – Т. 11. – С. e15847. doi: 10.7717/peerj.15847;
  26. Katayama Y. et al. Jumping the barrier to β-lactam resistance in Staphylococcus aureus //Journal of bacteriology. – 2003. – Т. 185. – №. 18. – С. 5465-5472. doi: 10.1128/JB.185.18.5465-5472.2003;
  27. Guo Y. H. et al. Population structure of food-borne Staphylococcus aureus in China //Zhonghua liu xing bing xue za zhi= Zhonghua liuxingbingxue zazhi. – 2023. – Т. 44. – №. 6. – С. 982-989. doi: 10.3760/cma.j.cn112338-20221206-01043;
  28. Sadat A. et al. Prevalence and characterization of PVL-positive Staphylococcus aureus isolated from raw cow’s milk //Toxins. – 2022. – Т. 14. – №. 2. – С. 97. https://doi.org/10.3390/toxins14020097;
  29. Beier R. C. 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. – Т. 9. – №. 11. – С. 2401. doi: 10.3390/microorganisms9112401;
  30. Park S., Ronholm J. Staphylococcus aureus in agriculture: lessons in evolution from a multispecies pathogen //Clinical microbiology reviews. – 2021. – Т. 34. – №. 2. – С. 10.1128/cmr. 00182-20. doi: 10.1128/CMR.00182-20;
  31. Pérez-Boto D. et al. Staphylococcus aureus in the processing environment of cured meat products //Foods. – 2023. – Т. 12. – №. 11. – С. 2161. doi: 10.3390/foods12112161;
  32. Naorem R. S. et al. Comparative analysis of prophages carried by human and animal-associated Staphylococcus aureus strains spreading across the European regions //Scientific Reports. – 2021. – Т. 11. – №. 1. – С. 18994. doi: 10.1038/s41598-021-98432-8;
  33. Wang H. 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. – Т. 11. – №. 15. – С. 2185. doi: 10.3390/foods11152185;
  34. Zhu Z. et al. Prevalence and virulence determinants of Staphylococcus aureus in wholesale and Retail Pork in Wuhan, Central China //Foods. – 2022. – Т. 11. – №. 24. – С. 4114. doi: 10.3390/foods11244114;
  35. Lowder B. V. et al. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus //Proceedings of the National Academy of Sciences. – 2009. – Т. 106. – №. 46. – С. 19545-19550. doi: 10.1073/pnas.0909285106;
  36. El-Telbany M. et al. Potential application of phage vB_EfKS5 to control Enterococcus faecalis and its biofilm in food //AMB Express. – 2023. – Т. 13. – №. 1. – С. 130. doi: 10.1186/s13568-023-01628-6;
  37. Holman D. B. et al. Antimicrobial resistance in Enterococcus spp. isolated from a beef processing plant and retail ground beef //Microbiology Spectrum. – 2021. – Т. 9. – №. 3. – С. e01980-21. doi: 10.1128/Spectrum.01980-21;
  38. Wei, Lei et al. “Prevalence and Genetic Diversity of Enterococcus faecalis Isolates from Mineral Water and Spring Water in China.” Frontiers in microbiology vol. 8 1109. 16 Jun. 2017, doi: 10.3389/fmicb.2017.01109;
  39. Wei L. et al. Prevalence and genetic diversity of Enterococcus faecalis isolates from mineral water and spring water in China //Frontiers in microbiology. – 2017. – Т. 8. – С. 1109. doi: 10.3389/fmicb.2023.1254896;
  40. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 13.0, 2024. (Abalable at: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_13.0_Breakpoint_Tables.pdf Accessed: 21.06.2024);
  41. Gołaś-Prądzyńska M., Łuszczyńska M., Rola J. G. Dairy Products: a potential source of Multidrug-Resistant Enterococcus faecalis and Enterococcus faecium Strains //Foods. – 2022. – Т. 11. – №. 24. – С. 4116. doi: 10.3390/foods11244116;
  42. Li J. et al. Molecular characterization of antimicrobial resistance and virulence factors of Enterococcus faecalis from ducks at slaughterhouses //Poultry Science. – 2022. – Т. 101. – №. 4. – С. 101646. doi: 10.1016/j.psj.2021.101646;
  43. EFSA Panel on Animal Health and Welfare (AHAW) 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. – Т. 15. – №. 8. – С. e04957. doi: 10.2903/j.efsa.2022.7127;
  44. Kim E. 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. – Т. 22. – №. 21. – С. 11335. doi: 10.3390/ijms222111335;
  45. Zheng J. X. et al. Characteristics of and virulence factors associated with biofilm formation in clinical Enterococcus faecalis isolates in China //Frontiers in microbiology. – 2017. – Т. 8. – С. 272233. doi: 10.3389/fmicb.2017.02338;
  46. Farias B. O. et al. First Report of a Wastewater Treatment-Adapted Enterococcus faecalis ST21 Harboring vanA Gene in Brazil //Current Microbiology. – 2023. – Т. 80. – №. 9. – С. 313. https://doi.org/10.1007/s00284-023-03418-6;
  47. Neumann B. et al. A core genome multilocus sequence typing scheme for Enterococcus faecalis //Journal of clinical microbiology. – 2019. – Т. 57. – №. 3. – С. 10.1128. doi: 10.1128/JCM.01686-18;
  48. Zaitseva E. A. et al. Clinical and microbiological aspects of Enterococcus faecalis-associated urinary tract infection //Russian Journal of Infection and Immunity. – 2021. – Т. 11. – №. 1. – С. 184-190. https://doi.org/10.34215/1609-1175-2023-1-75-80;
  49. Pöntinen A. K. et al. Apparent nosocomial adaptation of Enterococcus faecalis predates the modern hospital era //Nature communications. – 2021. – Т. 12. – №. 1. – С. 1523. https://doi.org/10.1038/s41467-021-21749-5;
  50. Moles L. et al. Preterm infant gut colonization in the neonatal ICU and complete restoration 2 years later //Clinical Microbiology and Infection. – 2015. – Т. 21. – №. 10. – С. 936. e1-936. e10. https://doi.org/10.1016/j.cmi.2015.06.003;
  51. Biggel M. et al. Spread of vancomycin-resistant Enterococcus faecium ST133 in the aquatic environment in Switzerland //Journal of Global Antimicrobial Resistance. – 2021. – Т. 27. – С. 31-36. https://doi.org/10.1016/j.jgar.2021.08.002;

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