Detection of Methicillin-resistant Staphylococcus aureus (MRSA) resistant to vancomycin and linezolid in bulk tank milk by E-test method

Öz

Staphylococcus aureus is considered a serious threat to public health, besides is one of the most common causes of subclinical mastitis in dairy cows. Therefore, especially methicillin-resistant Staphylococcus aureus (MRSA) is among the most critical reasons for antibiotic treatment. Monitoring the antibiotic resistance of MRSA from livestock animals and foods is of great significance. The E-test method is a suitable option for detecting antibiotics' minimum inhibition concentration (MIC) value because it is an easy and fast assay to perform. This study aimed to detect vancomycin, teicoplanin, and linezolid resistance of milk-borne 34 MRSA isolates with subclinical mastitis by the E-test method to determine MIC values. The study determined that 8.8% of MRSA isolates isolated from milk with subclinical mastitis were also resistant to vancomycin and 11.7% to linezolid, while none of the isolates were determined to be resistant to teicoplanin, according to EUCAST. The data obtained from the study reveal that the efficacy of vancomycin and linezolid antibiotics, which are commonly used against MRSA infections, are in danger. Especially before MRSA treatment, MIC values of antibiotics should be determined, and appropriate antibiotics should be used in effective doses.

Anahtar Kelimeler

• Antibiotic resistance
• Vancomycin-resistant S. aureus
• Linezolid-resistant S. aureus
• E-test

Kaynakça

1. 1. Adegoke, A. A., & Okoh, A. I. (2014). Species diversity and antibiotic resistance properties of Staphylococcus of farm animal origin in Nkonkobe Municipality, South Africa. Folia Microbiologica, 59, 133-140. https://doi.org/10.1007/s12223-013-0275-1
2. 3. Al-Amery, K., Elhariri, M., Elsayed, A., El-Moghazy, G., Elhelw, R., El-Mahallawy, H., El Hariri, M., & Hamza, D. (2019). Vancomycin-resistant Staphylococcus aureus isolated from camel meat and slaughterhouse workers in Egypt. Antimicrobial Resistance & Infection Control, 8, 1-8. https://doi.org/10.1186/s13756-019-0585-4 3.5. Aires-de-Sousa, M. (2017). Methicillin-resistant Staphylococcus aureus among animals: current overview. Clinical Microbiology and Infection, 23(6), 373-380. https://doi.org/10.1016/j.cmi.2016.11.002
3. 6. Algammal, A. M., Enany, M. E., El-Tarabili, R. M., Ghobashy, M. O., & Helmy, Y. A. (2020). Prevalence, antimicrobial resistance profiles, virulence and enterotoxins-determinant genes of MRSA isolated from subclinical bovine mastitis in Egypt. Pathogens, 9(5), 362. https://doi.org/10.3390/pathogens9050362
4. 8. Bouzidi, S., Bourabah, A., Cheriet, S., Abbassi, M. S., Meliani, S., & Bouzidi, H. (2023). Occurrence of virulence genes and methicillin-resistance in Staphylococcus aureus isolates causing subclinical bovine mastitis in Tiaret area, Algeria. Letters in Applied Microbiology. ovad003, https://doi.org/10.1093/lambio/ovad003 10. Campos, B., Pickering, A. C., Rocha, L. S., Aguilar, A. P., Fabres-Klein, M. H., de Oliveira Mendes, T. A., Fitzgerald, J. R. & & de Oliveira Barros Ribon, A. (2022). Diversity and pathogenesis of Staphylococcus aureus from bovine mastitis: current understanding and future perspectives. BMC Veterinary Research, 18(1), 1-16. https://doi.org/10.1186/s12917-022-03197-5
5. 12. Centers for Disease Control and Prevention (2019). 2019 AR Threats Report. https://www.cdc.gov/drugresistance/biggest-threats.html 14. Charlton, C. L., Hindler, J. A., Turnidge, J., & Humphries, R. M. (2014). Precision of vancomycin and daptomycin MICs for methicillin-resistant Staphylococcus aureus and effect of subculture and storage. Journal of Clinical Microbiology, 52(11), 3898-3905. https://doi.org/10.1128/JCM.01571-14
6. Clinical and Laboratory Standards Institute. (2023). M100. Performance standards for antimicrobial susceptibility testing, 33rd edition. https://clsi.org/standards/products/microbiology/documents/m100/
7. 17. Cui, L., Tominaga, E., Neoh, H. M., & Hiramatsu, K. (2006). Correlation between reduced daptomycin susceptibility and vancomycin resistance in vancomycin-intermediate Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 50(3), 1079-1082. https://doi.org/10.1128/AAC.50.3.1079-1082.2006
8. 19. European Committee on Antimicrobial Susceptibility Testing. (2023). According to EUCAST breakpoint tables for interpretation of MICs and zone diameters version 13.0, 2023. https://www.eucast.org/clinical_breakpoints

9. 21. Goerge, T., Lorenz, M. B., van Alen, S., Hübner, N. O., Becker, K., & Köck, R. (2017). MRSA colonization and infection among persons with occupational livestock exposure in Europe: prevalence, preventive options and evidence. Veterinary Microbiology, 200, 6-12. https://doi.org/10.1016/j.vetmic.2015.10.027
10. 23. Humphries, R. M., Pollett, S., & Sakoulas, G. (2013). A current perspective on daptomycin for the clinical microbiologist. Clinical microbiology reviews, 26(4), 759-780. https://doi.org/10.1128/CMR.00030-13 25. Kadariya, J., Smith, T. C., & Thapaliya, D. (2014). Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. BioMed Research International, 2014. Article ID 827965. https://doi.org/10.1155/2014/827965
11. 27. Keyvan, E., Yurdakul, O., Demirtas, A., Yalcin, H., & Bilgen, N. (2020). Identification of methicillin-resistant Staphylococcus aureus in bulk tank milk. Food Science and Technology, 40(1), 150-156. https://doi.org/10.1590/fst.35818
12. 29. Leão, C., Clemente, L., Cara d’Anjo, M., Albuquerque, T., & Amaro, A. (2022). Emergence of cfr-mediated linezolid resistance among livestock-associated Methicillin-Resistant Staphylococcus aureus (LA-MRSA) from Healthy Pigs in Portugal. Antibiotics, 11(10), 1439. https://doi.org/10.3390/antibiotics11101439 31. Lee, J. H., Choi, M. G., Park, H. J., Kim, H. C., & Choi, C. M. (2022). Comparison of mortality and clinical failure rates between vancomycin and teicoplanin in patients with methicillin-resistant Staphylococcus aureus pneumonia. BMC Infectious Diseases, 22(1), 1-10. https://doi.org/10.1186/s12879-022-07549-2
13. 33. Lienen, T., Grobbel, M., Tenhagen, B. A., & Maurischat, S. (2022). Plasmid-Coded Linezolid Resistance in Methicillin-Resistant Staphylococcus aureus from Food and Livestock in Germany. Antibiotics, 11(12), 1802. https://doi.org/10.3390/antibiotics11121802
14. 35. Mamfe, L. M., Akwuobu, C. A., & Ngbede, E. O. (2021). Phenotypic detection, antimicrobial susceptibility and virulence profile of staphylococci in the pig production setting, Makurdi, Nigeria. Access Microbiology, 3(12), 293. https://doi.org/10.1099/acmi.0.000293
15. 37. Maor, Y., Hagin, M., Belausov, N., Keller, N., Ben-David, D., & Rahav, G. (2009). Clinical features of heteroresistant vancomycin-intermediate Staphylococcus aureus bacteremia versus those of methicillin-resistant S. aureus bacteremia. The Journal of Infectious Diseases, 199(5), 619-624. https://doi.org/10.1086/596629
16. 39. Ozturk, D., Turutoglu, H., Pehlivanoglu, F., & Yapicier, O. S. (2019). Identification of bacteria isolated from dairy goats with subclinical mastitis and investigation of methicillin and vancomycin resistant Staphylococcus aureus strains. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 66(2), 191-196. https://doi.org/10.33988/auvfd.431465
17. 41. Phillips, C. J., Wells, N. A., Martinello, M., Smith, S., Woodman, R. J., & Gordon, D. L. (2016). Optimizing the detection of methicillin-resistant Staphylococcus aureus with elevated vancomycin minimum inhibitory concentrations within the susceptible range. Infection and drug resistance, 9, 87-92. https://doi.org/10.2147/IDR.S107961
18. 43. Saravolatz, L. D., & Pawlak, J. (2023). In vitro activity of fosfomycin alone and combination against Staphylococcus aureus with reduced susceptibility or resistance to methicillin, vancomycin, daptomycin or linezolid. Journal of Antimicrobial Chemotherapy, 78(1), 238-241. https://doi.org/10.1093/jac/dkac380 23.44. 45. Seegers, H., Fourichon, C., & Beaudeau, F. (2003). Production effects related to mastitis and mastitis economics in dairy cattle herds. Veterinary research, 34(5), 475-491. https://doi.org/10.1051/vetres:2003027
19. 47. Sergelidis, D., & Angelidis, A. S. (2017). Methicillin‐resistant Staphylococcus aureus: a controversial food‐borne pathogen. Letters in applied microbiology, 64(6), 409-418. https://doi.org/10.1111/lam.12735
20. 49. Soriano, A., Marco, F., Martínez, J. A., Pisos, E., Almela, M., Dimova, V. P., ... & Mensa, J. (2008). Influence of vancomycin minimum inhibitory concentration on the treatment of methicillin-resistant Staphylococcus aureus bacteremia. Clinical Infectious Diseases, 46(2), 193-200. https://doi.org/10.1086/524667 51. Stokes, M. B. (2017). Vancomycin in the kidney—a novel cast nephropathy. Journal of the American Society of Nephrology, 28(6), 1669-1670. https://doi.org/10.1681/ASN.2017010091
21. 53. Sukri, K. M., Mohamed, N. A., & Ilina Isahak, A. A. M. (2023). Prevalence and Susceptibility of Staphylococcus aureus Nasal Carriage Strains Isolated from Haemodialysis Patients. Malaysian Journal of Medicine and Health Sciences 19(1), 181-187. https://doi.org/10.47836/mjmhs19.1.25
22. 55. Svetitsky, S., Leibovici, L., & Paul, M. (2009). Comparative efficacy and safety of vancomycin versus teicoplanin: systematic review and meta-analysis. Antimicrobial Agents and Chemotherapy, 53(10), 4069-4079. https://doi.org/10.1128/AAC.00341-09
23. 57. Tandel, K., Praharaj, A. K., & Kumar, S. (2012). Differences in vancomycin MIC among MRSA isolates by agar dilution and E test method. Indian Journal of Medical Microbiology, 30(4), 453-455. https://doi.org/10.4103/0255-0857.103768
24. 59. Timmermans, M., Bogaerts, B., Vanneste, K., De Keersmaecker, S. C., Roosens, N. H., Kowalewicz, C., Simon, G., Argudín, M. A., Deplano, A., Hallin, M., Wattiau, P., Fretin, D., Denis, O., & Boland, C. (2022). Large diversity of linezolid-resistant isolates discovered in food-producing animals through linezolid selective monitoring in Belgium in 2019. Journal of Antimicrobial Chemotherapy, 77(1), 49-57. https://doi.org/10.1093/jac/dkab376
25. 61. Vanderhaeghen, W., Cerpentier, T., Adriaensen, C., Vicca, J., Hermans, K., & Butaye, P. (2010). Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Veterinary microbiology, 144(1-2), 166-171. https://doi.org/10.1016/j.vetmic.2009.12.044
26. 63. Yucel, N., Citak, S., & Bayhün, S. (2011). Antimicrobial resistance profile of Staphylococcus aureus isolated from clinical samples and foods of animal origin. Foodborne pathogens and disease, 8(3), 427-431. https://doi.org/10.1089/fpd.2010.0707