Investigation of the virulence, antibiotic resistance, and enterotoxin genes of methicillin-resistant Staphylococcus aureus (MRSA) isolated from nugget and salad samples
Abstract
Background and Objectives: Methicillin-resistant Staphylococcus aureus (MRSA) is a significant cause of illness from consuming contaminated food. MRSA is mainly known for its ability to develop resistance to antibiotics including methicillin. This research examined the antimicrobial resistance pattern, enterotoxigenic dispensation, virulence factors, and biotyping for MRSA isolates.
Materials and Methods: Susceptibility of S. aureus isolates to 13 types of antibiotics were assessed, and the genes associated with the resistance were investigated. Disk diffusion was used to identify the phenotypic tenet of antibiotic resistance. PCR is instrumental in detecting genes that confer resistance to antibiotics, virulence and enterotoxin genes.
Results: S. aureus were found in 167 out of 363 nugget and salad samples, representing 46% of the total sample count. Seventy-eight isolates (46.71%) were identified as MRSA bacteria. Its prevalence in different sources was as follows: 10% in bovine, 0% in ovine, 30% in poultry, and 56% in humans. MRSA displays high prevalence of resistance to cefotaxime and tetracycline (100%). coa was the most prevalent virulence factor (100%) in MRSA.
Conclusion: Distribution of antibiotic resistance genes in MRSA, highlights a serious health issue, as the presence of different antibiotic resistance genes exacerbates multidrug resistance in MRSA isolates.
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3. Deng Y, Liu J, Peters BM, Chen L, Miao J, Li B, et al. Antimicrobial resistance investigation on Staphylococcus strains in a local hospital in Guangzhou, China, 2001-2010. Microb Drug Resist 2015; 21: 102-104.
4. Miao J, Chen L, Wang J, Wang W, Chen D, Li L, et al. Current methodologies on genotyping for nosocomial pathogen methicillin-resistant Staphylococcus aureus (MRSA). Microb Pathog 2017; 107: 17-28.
5. Bai X, Nakatsu CH, Bhunia AK. Bacterial Biofilms and their Implications in pathogenesis and food safety. Foods 2021; 10: 2117.
6. Gouran ST, Doosti A, Jami MS. Brucella abortus antigen omp25 vaccines: development and targeting based on Lactococcus lactis. Vet Med Sci 2023; 9: 1908-1922.
7. Hasanpour Dehkordi A, Khaji L, Sakhaei Shahreza MH, Mashak Z, Safarpoor Dehkordi F, Safaee Y, et al. One-year prevalence of antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus recovered from raw meat. Trop Biomed 2017; 34: 396-404.
8. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015; 28: 603-661.
9. Puah SM, Chua KH, Tan JA. Virulence Factors and Antibiotic susceptibility of Staphylococcus aureus isolates in Ready-to-Eat Foods: Detection of S. aureus Contamination and a high Prevalence of Virulence Genes. Int J Environ Res Public Health 2016; 13: 199.
10. Lai YH, Chung YA, Wu YC, Fang CT, Chen PJ. Disease burden from foodborne illnesses in Taiwan, 2012-2015. J Formos Med Assoc 2020; 119: 1372-1381.
11. Fusco V, Quero GM, Morea M, Blaiotta G, Visconti A. Rapid and reliable identification of Staphylococcus aureus harbouring the enterotoxin gene cluster (egc) and quantitative detection in raw milk by real time PCR. Int J Food Microbiol 2011; 144: 528-537.
12. Tirbakhsh Gouran S, Doosti A, Jami MS. Expression of Brucella abortus Omp25 protein in Lactococcus lactis probiotic bacteria. J Mazandaran Univ Med Sci 2023; 32: 16-31.
13. 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.
14. Safarpour-Dehkordi M, Chabok O, Asgari M, Khademi R, Doosti A. A comprehensive investigation of the medicinal efficacy of antimicrobial fusion peptides expressed in probiotic bacteria for the treatment of pan drug-resistant (PDR) infections. Arch Microbiol 2024; 206: 93.
15. Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 2009; 7: 629-641.
16. Silva V, Araújo S, Monteiro A, Eira J, Pereira JE, Maltez L, et al. Staphylococcus aureus and MRSA in Livestock: Antimicrobial Resistance and Genetic Lineages. Microorganisms 2023; 11: 124.
17. Safarpour-Dehkordi M, Doosti A, Jami MS, Gholipour A. Quantitative Real Time PCR study on the effects of hilA gene deletion on the expression of pathogenicity genes in Salmonella enterica ssp. J BioSci Biotechnol 2018; 7: 73-78.
18. Wang X, Li G, Xia X, Yang B, Xi M, Meng J. Antimicrobial susceptibility and molecular typing of methicillin-resistant Staphylococcus aureus in retail foods in Shaanxi, China. Foodborne Pathog Dis 2014; 11: 281-286.
19. Islam MA, Parveen S, Rahman M, Huq M, Nabi A, Khan ZUM, et al. Occurrence and Characterization of Methicillin Resistant Staphylococcus aureus in Processed Raw Foods and Ready-to-Eat Foods in an Urban Setting of a Developing Country. Front Microbiol 2019; 10: 503.
20. Fusco V, Chieffi D, Fanelli F, Logrieco AF, Cho GS, Kabisch J, et al. Microbial quality and safety of milk and milk products in the 21st century. Compr Rev Food Sci Food Saf 2020; 19: 2013-2049.
21. Petinaki E, Spiliopoulou I. Methicillin-resistant Staphylococcus aureus among companion and food-chain animals: impact of human contacts. Clin Microbiol Infect 2012; 18: 626-634.
22. Osman K, Badr J, Al-Maary KS, Moussa IM, Hessain AM, Girah ZM, et al. Prevalence of the antibiotic resistance genes in Coagulase-Positive-and Negative-Staphylococcus in chicken meat retailed to Consumers. Front Microbiol 2016; 7: 1846.
23. Fijałkowski K, Peitler D, Karakulska J. Staphylococci isolated from ready-to-eat meat - Identification, antibiotic resistance and toxin gene profile. Int J Food Microbiol 2016; 238: 113-120.
24. Morales P, Tang P, Mariano E, Gopalan A, Aji N, Pérez-López A, et al. Evaluation of direct Antimicrobial Susceptibility testing of Gram-Negative Bacilli and Staphylococcus aureus from positive Pediatric blood Culture Bottles using BD phoenix M50. Microorganisms 2024; 12: 1704.
25. Farah IO, Pedersen E, Halgaard C, Bruhn K. Comparative characterization and biotyping of Staphylococcus aureus isolates from human and bovine sources. Acta Vet Scand 1988; 29: 303-310.
26. Selb R, Jansen K, Eckardt M, Tamminga T, Dudareva S, Gassowski M, et al. External quality assessment (EQA) of Neisseria gonorrhoeae antimicrobial susceptibility testing in primary laboratories in Germany. BMC Infect Dis 2020; 20: 514.
27. Ranjbar R, Farsani FY, Dehkordi FS. Phenotypic analysis of antibiotic resistance and genotypic study of the vacA, cagA, iceA, oipA and babA genotypes of the Helicobacter pylori strains isolated from raw milk. Antimicrob Resist Infect Control 2018; 7: 115.
28. Gutiérrez D, Delgado S, Vázquez-Sánchez D, Martínez B, Cabo ML, Rodríguez A, et al. Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Appl Environ Microbiol 2012; 78: 8547-8554.
29. Castro A, Santos C, Meireles H, Silva J, Teixeira P. Food handlers as potential sources of dissemination of virulent strains of Staphylococcus aureus in the community. J Infect Public Health 2016; 9: 153-160.
30. Costa WL, Ferreira Jdos S, Carvalho JS, Cerqueira ES, Oliveira LC, Almeida RC. Methicillin-resistant Staphylococcus aureus in raw meats and prepared foods in public hospitals in salvador, Bahia, Brazil. J Food Sci 2015; 80: M147-M150.
31. Castro A, Santos C, Meireles H, Silva J, Teixeira P. Food handlers as potential sources of dissemination of virulent strains of Staphylococcus aureus in the community. J Infect Public Health 2016; 9: 153-160.
32. Torres Segarra SM, Pacheco Cárdenas KE. Methicillin-resistant Staphylococcus aureus in food. Vive Rev Salud 2021; 4: 23-35.
33. Kitai S, Shimizu A, Kawano J, Sato E, Nakano C, Kitagawa H, et al. Prevalence and characterization of Staphylococcus aureus and enterotoxigenic Staphylococcus aureus in retail raw chicken meat throughout Japan. J Vet Med Sci 2005; 67: 269-274.
34. Normanno G, La Salandra G, Dambrosio A, Quaglia NC, Corrente M, Parisi A, et al. Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. Int J Food Microbiol 2007; 115: 290-296.
35. Mbindyo CM, Gitao GC, Plummer PJ, Kulohoma BW, Mulei CM, Bett R. Antimicrobial resistance profiles and genes of Staphylococci isolated from Mastitic Cow's milk in Kenya. Antibiotics (Basel) 2021; 10: 772.
36. Martin JG, de Oliveira E Silva G, da Fonseca CR, Morales CB, Souza Pamplona Silva C, Miquelluti DL, et al. Efficiency of a cleaning protocol for the removal of enterotoxigenic Staphylococcus aureus strains in dairy plants. Int J Food Microbiol 2016; 238: 295-301.
37. Wu S, Huang J, Wu Q, Zhang F, Zhang J, Lei T, et al. Prevalence and characterization of Staphylococcus aureus isolated from Retail Vegetables in China. Front Microbiol 2018; 9: 1263.
38. González-Machado C, Alonso-Calleja C, Capita R. Methicillin-resistant Staphylococcus aureus (MRSA) in different food groups and drinking water. Foods 2024; 13: 2686.
39. Abdolmaleki Z, Mashak Z, Safarpoor Dehkordi F. Phenotypic and genotypic characterization of antibiotic resistance in the methicillin-resistant Staphylococcus aureus strains isolated from hospital cockroaches. Antimicrob Resist Infect Control 2019; 8: 54.
40. Kim MJ, Cheigh CI. Microbiological contamination of fresh-cut produce in Korea. Food Sci Biotechnol 2021; 31: 79-87.
41. Rahi A, Kazemeini H, Jafariaskari S, Seif A, Hosseini S, Safarpoor Dehkordi F. Genotypic and phenotypic-based assessment of antibiotic resistance and profile of Staphylococcal cassette chromosome mec in the methicillin-resistant Staphylococcus aureus recovered from raw milk. Infect Drug Resist 2020; 13: 273-283.
42. Ngemenya MN, Djeukem GGR, Nyongbela KD, Bate PNN, Babiaka SB, Monya E, et al. Microbial, phytochemical, toxicity analyses and antibacterial activity against multidrug resistant bacteria of some traditional remedies sold in Buea Southwest Cameroon. BMC Complement Altern Med 2019; 19: 150.
2. 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 (Basel) 2021; 10: 1108.
3. Deng Y, Liu J, Peters BM, Chen L, Miao J, Li B, et al. Antimicrobial resistance investigation on Staphylococcus strains in a local hospital in Guangzhou, China, 2001-2010. Microb Drug Resist 2015; 21: 102-104.
4. Miao J, Chen L, Wang J, Wang W, Chen D, Li L, et al. Current methodologies on genotyping for nosocomial pathogen methicillin-resistant Staphylococcus aureus (MRSA). Microb Pathog 2017; 107: 17-28.
5. Bai X, Nakatsu CH, Bhunia AK. Bacterial Biofilms and their Implications in pathogenesis and food safety. Foods 2021; 10: 2117.
6. Gouran ST, Doosti A, Jami MS. Brucella abortus antigen omp25 vaccines: development and targeting based on Lactococcus lactis. Vet Med Sci 2023; 9: 1908-1922.
7. Hasanpour Dehkordi A, Khaji L, Sakhaei Shahreza MH, Mashak Z, Safarpoor Dehkordi F, Safaee Y, et al. One-year prevalence of antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus recovered from raw meat. Trop Biomed 2017; 34: 396-404.
8. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015; 28: 603-661.
9. Puah SM, Chua KH, Tan JA. Virulence Factors and Antibiotic susceptibility of Staphylococcus aureus isolates in Ready-to-Eat Foods: Detection of S. aureus Contamination and a high Prevalence of Virulence Genes. Int J Environ Res Public Health 2016; 13: 199.
10. Lai YH, Chung YA, Wu YC, Fang CT, Chen PJ. Disease burden from foodborne illnesses in Taiwan, 2012-2015. J Formos Med Assoc 2020; 119: 1372-1381.
11. Fusco V, Quero GM, Morea M, Blaiotta G, Visconti A. Rapid and reliable identification of Staphylococcus aureus harbouring the enterotoxin gene cluster (egc) and quantitative detection in raw milk by real time PCR. Int J Food Microbiol 2011; 144: 528-537.
12. Tirbakhsh Gouran S, Doosti A, Jami MS. Expression of Brucella abortus Omp25 protein in Lactococcus lactis probiotic bacteria. J Mazandaran Univ Med Sci 2023; 32: 16-31.
13. 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.
14. Safarpour-Dehkordi M, Chabok O, Asgari M, Khademi R, Doosti A. A comprehensive investigation of the medicinal efficacy of antimicrobial fusion peptides expressed in probiotic bacteria for the treatment of pan drug-resistant (PDR) infections. Arch Microbiol 2024; 206: 93.
15. Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 2009; 7: 629-641.
16. Silva V, Araújo S, Monteiro A, Eira J, Pereira JE, Maltez L, et al. Staphylococcus aureus and MRSA in Livestock: Antimicrobial Resistance and Genetic Lineages. Microorganisms 2023; 11: 124.
17. Safarpour-Dehkordi M, Doosti A, Jami MS, Gholipour A. Quantitative Real Time PCR study on the effects of hilA gene deletion on the expression of pathogenicity genes in Salmonella enterica ssp. J BioSci Biotechnol 2018; 7: 73-78.
18. Wang X, Li G, Xia X, Yang B, Xi M, Meng J. Antimicrobial susceptibility and molecular typing of methicillin-resistant Staphylococcus aureus in retail foods in Shaanxi, China. Foodborne Pathog Dis 2014; 11: 281-286.
19. Islam MA, Parveen S, Rahman M, Huq M, Nabi A, Khan ZUM, et al. Occurrence and Characterization of Methicillin Resistant Staphylococcus aureus in Processed Raw Foods and Ready-to-Eat Foods in an Urban Setting of a Developing Country. Front Microbiol 2019; 10: 503.
20. Fusco V, Chieffi D, Fanelli F, Logrieco AF, Cho GS, Kabisch J, et al. Microbial quality and safety of milk and milk products in the 21st century. Compr Rev Food Sci Food Saf 2020; 19: 2013-2049.
21. Petinaki E, Spiliopoulou I. Methicillin-resistant Staphylococcus aureus among companion and food-chain animals: impact of human contacts. Clin Microbiol Infect 2012; 18: 626-634.
22. Osman K, Badr J, Al-Maary KS, Moussa IM, Hessain AM, Girah ZM, et al. Prevalence of the antibiotic resistance genes in Coagulase-Positive-and Negative-Staphylococcus in chicken meat retailed to Consumers. Front Microbiol 2016; 7: 1846.
23. Fijałkowski K, Peitler D, Karakulska J. Staphylococci isolated from ready-to-eat meat - Identification, antibiotic resistance and toxin gene profile. Int J Food Microbiol 2016; 238: 113-120.
24. Morales P, Tang P, Mariano E, Gopalan A, Aji N, Pérez-López A, et al. Evaluation of direct Antimicrobial Susceptibility testing of Gram-Negative Bacilli and Staphylococcus aureus from positive Pediatric blood Culture Bottles using BD phoenix M50. Microorganisms 2024; 12: 1704.
25. Farah IO, Pedersen E, Halgaard C, Bruhn K. Comparative characterization and biotyping of Staphylococcus aureus isolates from human and bovine sources. Acta Vet Scand 1988; 29: 303-310.
26. Selb R, Jansen K, Eckardt M, Tamminga T, Dudareva S, Gassowski M, et al. External quality assessment (EQA) of Neisseria gonorrhoeae antimicrobial susceptibility testing in primary laboratories in Germany. BMC Infect Dis 2020; 20: 514.
27. Ranjbar R, Farsani FY, Dehkordi FS. Phenotypic analysis of antibiotic resistance and genotypic study of the vacA, cagA, iceA, oipA and babA genotypes of the Helicobacter pylori strains isolated from raw milk. Antimicrob Resist Infect Control 2018; 7: 115.
28. Gutiérrez D, Delgado S, Vázquez-Sánchez D, Martínez B, Cabo ML, Rodríguez A, et al. Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Appl Environ Microbiol 2012; 78: 8547-8554.
29. Castro A, Santos C, Meireles H, Silva J, Teixeira P. Food handlers as potential sources of dissemination of virulent strains of Staphylococcus aureus in the community. J Infect Public Health 2016; 9: 153-160.
30. Costa WL, Ferreira Jdos S, Carvalho JS, Cerqueira ES, Oliveira LC, Almeida RC. Methicillin-resistant Staphylococcus aureus in raw meats and prepared foods in public hospitals in salvador, Bahia, Brazil. J Food Sci 2015; 80: M147-M150.
31. Castro A, Santos C, Meireles H, Silva J, Teixeira P. Food handlers as potential sources of dissemination of virulent strains of Staphylococcus aureus in the community. J Infect Public Health 2016; 9: 153-160.
32. Torres Segarra SM, Pacheco Cárdenas KE. Methicillin-resistant Staphylococcus aureus in food. Vive Rev Salud 2021; 4: 23-35.
33. Kitai S, Shimizu A, Kawano J, Sato E, Nakano C, Kitagawa H, et al. Prevalence and characterization of Staphylococcus aureus and enterotoxigenic Staphylococcus aureus in retail raw chicken meat throughout Japan. J Vet Med Sci 2005; 67: 269-274.
34. Normanno G, La Salandra G, Dambrosio A, Quaglia NC, Corrente M, Parisi A, et al. Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. Int J Food Microbiol 2007; 115: 290-296.
35. Mbindyo CM, Gitao GC, Plummer PJ, Kulohoma BW, Mulei CM, Bett R. Antimicrobial resistance profiles and genes of Staphylococci isolated from Mastitic Cow's milk in Kenya. Antibiotics (Basel) 2021; 10: 772.
36. Martin JG, de Oliveira E Silva G, da Fonseca CR, Morales CB, Souza Pamplona Silva C, Miquelluti DL, et al. Efficiency of a cleaning protocol for the removal of enterotoxigenic Staphylococcus aureus strains in dairy plants. Int J Food Microbiol 2016; 238: 295-301.
37. Wu S, Huang J, Wu Q, Zhang F, Zhang J, Lei T, et al. Prevalence and characterization of Staphylococcus aureus isolated from Retail Vegetables in China. Front Microbiol 2018; 9: 1263.
38. González-Machado C, Alonso-Calleja C, Capita R. Methicillin-resistant Staphylococcus aureus (MRSA) in different food groups and drinking water. Foods 2024; 13: 2686.
39. Abdolmaleki Z, Mashak Z, Safarpoor Dehkordi F. Phenotypic and genotypic characterization of antibiotic resistance in the methicillin-resistant Staphylococcus aureus strains isolated from hospital cockroaches. Antimicrob Resist Infect Control 2019; 8: 54.
40. Kim MJ, Cheigh CI. Microbiological contamination of fresh-cut produce in Korea. Food Sci Biotechnol 2021; 31: 79-87.
41. Rahi A, Kazemeini H, Jafariaskari S, Seif A, Hosseini S, Safarpoor Dehkordi F. Genotypic and phenotypic-based assessment of antibiotic resistance and profile of Staphylococcal cassette chromosome mec in the methicillin-resistant Staphylococcus aureus recovered from raw milk. Infect Drug Resist 2020; 13: 273-283.
42. Ngemenya MN, Djeukem GGR, Nyongbela KD, Bate PNN, Babiaka SB, Monya E, et al. Microbial, phytochemical, toxicity analyses and antibacterial activity against multidrug resistant bacteria of some traditional remedies sold in Buea Southwest Cameroon. BMC Complement Altern Med 2019; 19: 150.
| Files | ||
| Issue | Vol 17 No 5 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i5.19890 | |
| Keywords | ||
| Methicillin-resistant Staphylococcus aureus Antibiotic resistance Enterotoxin genes Nugget Salad Polymerase chain reaction | ||
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How to Cite
1.
Vahed Dehkordi N, Rahimi E. Investigation of the virulence, antibiotic resistance, and enterotoxin genes of methicillin-resistant Staphylococcus aureus (MRSA) isolated from nugget and salad samples. Iran J Microbiol. 2025;17(5):814-825.
