Prevalence, antimicrobial resistance, virulence gene distribution and SCCmec typing of methicillin-resistant Staphylococcus aureus isolated from raw milk and dairy products
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Abstract
Background and Objectives: Researchers have focused on Staphylococcus aureus because it is transmitted through food, such as milk and dairy products, and causes human diseases. Prevalence, antimicrobial resistance, presence, and distribution of methicillin-resistant S. aureus (MRSA) virulence genes isolated from raw milk and dairy products were evaluated.
Materials and Methods: 300 samples of dairy products were collected from Shahrekord, Iran. S. aureus was identified using biochemical tests and screened for sensitivity to 13 antibiotics to identify resistance genes. In addition, SCCmec typing was performed.
Results: Out of 300, S. aureus was found in 82 samples. Raw milk had the highest contamination with S. aureus (60 of 82), followed by cheese (15 of 82), and butter (7 of 82). At least one resistance gene was present in every isolate of S. aureus. Virulence factors and enterotoxin-coding genes, such as sea, seb, sec, and sed were highly distributed.
Conclusion: The results of this study revealed the presence of toxin-producing MRSA strains in raw milk and dairy products. MRSA in dairy farms is an important risk factor for the spread of staphylococcal infections; therefore, further studies are needed to find strategies for controlling the presence of S. aureus, especially MRSA, in dairy products.
1. Hornik B, Czarny J, Staninska-Pięta J, Wolko Ł, Cyplik P, Piotrowska-Cyplik A. The raw milk microbiota from semi-subsistence farms characteristics by NGS analysis method. Molecules 2021; 26: 5029.
2. Spanu V, Spanu C, Virdis S, Cossu F, Scarano C, De Santis EP. Virulence factors and genetic variability of Staphylococcus aureus strains isolated from raw sheep's milk cheese. Int J Food Microbiol 2012; 153: 53-57.
3. Riva A, Borghi E, Cirasola D, Colmegna S, Borgo F, Amato E, et al. Methicillin-resistant Staphylococcus aureus in raw milk: prevalence, SCCmec typing, enterotoxin characterization, and antimicrobial resistance patterns. J Food Prot 2015; 78: 1142-1146.
4. Argudín MÁ, Mendoza MC, Rodicio MR. Food poisoning and Staphylococcus aureus enterotoxins.
Toxins (Basel) 2010; 2: 1751-1773.
5. Ortega E, Abriouel H, Lucas R, Gálvez A. Multiple roles of Staphylococcus aureus enterotoxins: pathogenicity, superantigenic activity, and correlation to antibiotic resistance. Toxins (Basel) 2010; 2: 2117-2131.
6. Fetsch A, Contzen M, Hartelt K, Kleiser A, Maassen S, Rau J, et al. Staphylococcus aureus food-poisoning outbreak associated with the consumption of ice-cream. Int J Food Microbiol 2014; 187: 1-6.
7. Lejeune JT, Rajala-Schultz PJ. Food safety: unpasteurized milk: a continued public health threat. Clin Infect Dis 2009; 48: 93-100.
8. Hornik B, Czarny J, Staninska-Pięta J, Wolko Ł, Cyplik P, Piotrowska-Cyplik A. The raw milk microbiota from semi-subsistence farms characteristics by NGS analysis method. Molecules 2021; 26: 5029.
9. Kayili E, Sanlibaba P. Prevalence, characterization and antibiotic resistance of Staphylococcus aureus isolated from traditional cheeses in Turkey. Int J Food Prop 2020; 23: 1441-1451.
10. Titouche Y, Akkou M, Houali K, Auvray F, Hennekinne JA. Role of milk and milk products in the spread of methicillin‐resistant Staphylococcus aureus in the dairy production chain. J Food Sci 2022; 87: 3699-3723.
11. Alp D, Bulantekin Ö. The microbiological quality of various foods dried by applying different drying methods: a review. Eur Food Res Technol 2021; 247: 1333-1343.
12. Menberu MA, Liu S, Cooksley C, Hayes AJ, Psaltis AJ, Wormald PJ, et al. Corynebacterium accolens has antimicrobial activity against Staphylococcus aureus and methicillin-resistant S. aureus pathogens isolated from the sinonasal niche of chronic rhinosinusitis patients. Pathogens 2021; 10: 207.
13. El-Zamkan MA, Mubarak AG, Ali AO. Prevalence and phylogenetic relationship among methicillin-and vancomycin-resistant Staphylococci isolated from hospital’s dairy food, food handlers, and patients. J Adv Vet Anim Res 2019; 6: 463-473.
14. Wu S, Huang J, Wu Q, Zhang J, Zhang F, Yang X, et al. Staphylococcus aureus isolated from retail meat and meat products in China: incidence, antibiotic resistance and genetic diversity. Front Microbiol 2018; 9: 2767.
15. Humphries R, Bobenchik AM, Hindler JA, Schuetz AN. Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st edition. J Clin Microbiol 2021; 59(12): e0021321.
16. Liu J, Chen D, Peters BM, Li L, Li B, Xu Z, et al. Staphylococcal chromosomal cassettes mec (SCCmec): A mobile genetic element in methicillin-resistant Staphylococcus aureus. Microb Pathog 2016; 101: 56-67.
17. McKay AM. Antimicrobial resistance and heat sensitivity of oxacillin-resistant, mecA-positive Staphylococcus spp. from unpasteurized milk. J Food Prot 2008; 71: 186-190.
18. Weinstein MP, Lewis JS 2nd. The clinical and laboratory standards institute subcommittee on antimicrobial susceptibility testing: background, organization, functions, and processes. J Clin Microbiol 2020; 58(3): e01864-19.
19. Lim SK, Nam HM, Jang GC, Lee HS, Jung SC, Kim TS. Transmission and persistence of methicillin-resistant Staphylococcus aureus in milk, environment, and workers in dairy cattle farms. Foodborne Pathog Dis 2013; 10: 731-736.
20. Basanisi MG, La Bella G, Nobili G, Franconieri I, La Salandra G. Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol 2017; 62: 141-146.
21. Kreausukon K, Fetsch A, Kraushaar B, Alt K, Müller K, Krömker V, et al. Prevalence, antimicrobial resistance, and molecular characterization of methicillin-resistant Staphylococcus aureus from bulk tank milk of dairy herds. J Dairy Sci 2012; 95: 4382-4388.
22. Paterson GK, Morgan FJ, Harrison EM, Cartwright EJ, Török ME, Zadoks RN, et al. Prevalence and characterization of human mecC methicillin-resistant Staphylococcus aureus isolates in England. J Antimicrob Chemother 2014; 69: 907-910.
23. Türkyılmaz S, Tekbıyık S, Oryasin E, Bozdogan B. Molecular epidemiology and antimicrobial resistance mechanisms of methicillin‐resistant Staphylococcus aureus isolated from bovine milk. Zoonoses Public Health 2010; 57: 197-203.
24. Hata E, Katsuda K, Kobayashi H, Uchida I, Tanaka K, Eguchi M. Genetic variation among Staphylococcus aureus strains from bovine milk and their relevance to methicillin-resistant isolates from humans. J Clin Microbiol 2010; 48: 2130-2139.
25. Mekhloufi OA, Chieffi D, Hammoudi A, Bensefia SA, Fanelli F, Fusco V. Prevalence, enterotoxigenic potential and antimicrobial resistance of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) isolated from Algerian ready to eat foods. Toxins (Basel) 2021; 13: 835.
26. Chieffi D, Fanelli F, Cho GS, Schubert J, Blaiotta G, Franz CMAP, et al. Novel insights into the enterotoxigenic potential and genomic background of Staphylococcus aureus isolated from raw milk. Food Microbiol 2020; 90: 103482.
27. Lv G, Jiang R, Zhang H, Wang L, Li L, Gao W, et al. Molecular characteristics of Staphylococcus aureus from food samples and food poisoning outbreaks in Shijiazhuang, China. Front Microbiol 2021; 12: 652276.
28. Jørgensen HJ, Mørk T, Høgåsen HR, Rørvik LM. Enterotoxigenic Staphylococcus aureus in bulk milk in Norway. J Appl Microbiol 2005; 99: 158-166.
29. Neder VE, Canavesio VR, Calvinho LF. Presence of enterotoxigenic Staphylococcus aureus in bulk tank milk from Argentine dairy farms. Rev Argent Microbiol 2011; 43: 104-106.
30. Ahmad-Mansour N, Loubet P, Pouget C, Dunyach-Remy C, Sotto A, Lavigne JP, et al. Staphylococcus aureus toxins: an update on their pathogenic properties and potential treatments. Toxins (Basel) 2021; 13: 677.
31. Liu S, Cai X, Xue W, Ma D, Zhang W. Chitosan derivatives co-delivering nitric oxide and methicillin for the effective therapy to the methicillin-resistant S. aureus infection. Carbohydr Polym 2020; 234: 115928.
2. Spanu V, Spanu C, Virdis S, Cossu F, Scarano C, De Santis EP. Virulence factors and genetic variability of Staphylococcus aureus strains isolated from raw sheep's milk cheese. Int J Food Microbiol 2012; 153: 53-57.
3. Riva A, Borghi E, Cirasola D, Colmegna S, Borgo F, Amato E, et al. Methicillin-resistant Staphylococcus aureus in raw milk: prevalence, SCCmec typing, enterotoxin characterization, and antimicrobial resistance patterns. J Food Prot 2015; 78: 1142-1146.
4. Argudín MÁ, Mendoza MC, Rodicio MR. Food poisoning and Staphylococcus aureus enterotoxins.
Toxins (Basel) 2010; 2: 1751-1773.
5. Ortega E, Abriouel H, Lucas R, Gálvez A. Multiple roles of Staphylococcus aureus enterotoxins: pathogenicity, superantigenic activity, and correlation to antibiotic resistance. Toxins (Basel) 2010; 2: 2117-2131.
6. Fetsch A, Contzen M, Hartelt K, Kleiser A, Maassen S, Rau J, et al. Staphylococcus aureus food-poisoning outbreak associated with the consumption of ice-cream. Int J Food Microbiol 2014; 187: 1-6.
7. Lejeune JT, Rajala-Schultz PJ. Food safety: unpasteurized milk: a continued public health threat. Clin Infect Dis 2009; 48: 93-100.
8. Hornik B, Czarny J, Staninska-Pięta J, Wolko Ł, Cyplik P, Piotrowska-Cyplik A. The raw milk microbiota from semi-subsistence farms characteristics by NGS analysis method. Molecules 2021; 26: 5029.
9. Kayili E, Sanlibaba P. Prevalence, characterization and antibiotic resistance of Staphylococcus aureus isolated from traditional cheeses in Turkey. Int J Food Prop 2020; 23: 1441-1451.
10. Titouche Y, Akkou M, Houali K, Auvray F, Hennekinne JA. Role of milk and milk products in the spread of methicillin‐resistant Staphylococcus aureus in the dairy production chain. J Food Sci 2022; 87: 3699-3723.
11. Alp D, Bulantekin Ö. The microbiological quality of various foods dried by applying different drying methods: a review. Eur Food Res Technol 2021; 247: 1333-1343.
12. Menberu MA, Liu S, Cooksley C, Hayes AJ, Psaltis AJ, Wormald PJ, et al. Corynebacterium accolens has antimicrobial activity against Staphylococcus aureus and methicillin-resistant S. aureus pathogens isolated from the sinonasal niche of chronic rhinosinusitis patients. Pathogens 2021; 10: 207.
13. El-Zamkan MA, Mubarak AG, Ali AO. Prevalence and phylogenetic relationship among methicillin-and vancomycin-resistant Staphylococci isolated from hospital’s dairy food, food handlers, and patients. J Adv Vet Anim Res 2019; 6: 463-473.
14. Wu S, Huang J, Wu Q, Zhang J, Zhang F, Yang X, et al. Staphylococcus aureus isolated from retail meat and meat products in China: incidence, antibiotic resistance and genetic diversity. Front Microbiol 2018; 9: 2767.
15. Humphries R, Bobenchik AM, Hindler JA, Schuetz AN. Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st edition. J Clin Microbiol 2021; 59(12): e0021321.
16. Liu J, Chen D, Peters BM, Li L, Li B, Xu Z, et al. Staphylococcal chromosomal cassettes mec (SCCmec): A mobile genetic element in methicillin-resistant Staphylococcus aureus. Microb Pathog 2016; 101: 56-67.
17. McKay AM. Antimicrobial resistance and heat sensitivity of oxacillin-resistant, mecA-positive Staphylococcus spp. from unpasteurized milk. J Food Prot 2008; 71: 186-190.
18. Weinstein MP, Lewis JS 2nd. The clinical and laboratory standards institute subcommittee on antimicrobial susceptibility testing: background, organization, functions, and processes. J Clin Microbiol 2020; 58(3): e01864-19.
19. Lim SK, Nam HM, Jang GC, Lee HS, Jung SC, Kim TS. Transmission and persistence of methicillin-resistant Staphylococcus aureus in milk, environment, and workers in dairy cattle farms. Foodborne Pathog Dis 2013; 10: 731-736.
20. Basanisi MG, La Bella G, Nobili G, Franconieri I, La Salandra G. Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol 2017; 62: 141-146.
21. Kreausukon K, Fetsch A, Kraushaar B, Alt K, Müller K, Krömker V, et al. Prevalence, antimicrobial resistance, and molecular characterization of methicillin-resistant Staphylococcus aureus from bulk tank milk of dairy herds. J Dairy Sci 2012; 95: 4382-4388.
22. Paterson GK, Morgan FJ, Harrison EM, Cartwright EJ, Török ME, Zadoks RN, et al. Prevalence and characterization of human mecC methicillin-resistant Staphylococcus aureus isolates in England. J Antimicrob Chemother 2014; 69: 907-910.
23. Türkyılmaz S, Tekbıyık S, Oryasin E, Bozdogan B. Molecular epidemiology and antimicrobial resistance mechanisms of methicillin‐resistant Staphylococcus aureus isolated from bovine milk. Zoonoses Public Health 2010; 57: 197-203.
24. Hata E, Katsuda K, Kobayashi H, Uchida I, Tanaka K, Eguchi M. Genetic variation among Staphylococcus aureus strains from bovine milk and their relevance to methicillin-resistant isolates from humans. J Clin Microbiol 2010; 48: 2130-2139.
25. Mekhloufi OA, Chieffi D, Hammoudi A, Bensefia SA, Fanelli F, Fusco V. Prevalence, enterotoxigenic potential and antimicrobial resistance of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) isolated from Algerian ready to eat foods. Toxins (Basel) 2021; 13: 835.
26. Chieffi D, Fanelli F, Cho GS, Schubert J, Blaiotta G, Franz CMAP, et al. Novel insights into the enterotoxigenic potential and genomic background of Staphylococcus aureus isolated from raw milk. Food Microbiol 2020; 90: 103482.
27. Lv G, Jiang R, Zhang H, Wang L, Li L, Gao W, et al. Molecular characteristics of Staphylococcus aureus from food samples and food poisoning outbreaks in Shijiazhuang, China. Front Microbiol 2021; 12: 652276.
28. Jørgensen HJ, Mørk T, Høgåsen HR, Rørvik LM. Enterotoxigenic Staphylococcus aureus in bulk milk in Norway. J Appl Microbiol 2005; 99: 158-166.
29. Neder VE, Canavesio VR, Calvinho LF. Presence of enterotoxigenic Staphylococcus aureus in bulk tank milk from Argentine dairy farms. Rev Argent Microbiol 2011; 43: 104-106.
30. Ahmad-Mansour N, Loubet P, Pouget C, Dunyach-Remy C, Sotto A, Lavigne JP, et al. Staphylococcus aureus toxins: an update on their pathogenic properties and potential treatments. Toxins (Basel) 2021; 13: 677.
31. Liu S, Cai X, Xue W, Ma D, Zhang W. Chitosan derivatives co-delivering nitric oxide and methicillin for the effective therapy to the methicillin-resistant S. aureus infection. Carbohydr Polym 2020; 234: 115928.
| Files | ||
| Issue | Vol 16 No 5 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i5.16793 | |
| Keywords | ||
| Methicillin-resistant Staphylococcus aureus; Drug resistance; Pathogenicity; Dairy products; Milk | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Vahed Dehkordi N, Rahimi E, Zia Jahromi N. Prevalence, antimicrobial resistance, virulence gene distribution and SCCmec typing of methicillin-resistant Staphylococcus aureus isolated from raw milk and dairy products. Iran J Microbiol. 2024;16(5):605-613.
