Prophage typing of Staphylococcus aureus in traditional dairy products of Ilam, Iran
,
Abstract
Background and Objectives: Antimicrobial resistance (AMR), particularly from methicillin-resistant Staphylococcus aureus (MRSA), poses a significant public health threat, exacerbated by antibiotic misuse in livestock and food production. This study aimed to evaluate the prevalence of MRSA in traditional dairy products from Ilam, Iran, and explore the role of prophages in enhancing bacterial virulence and resistance, assessing their implications for food safety.
Materials and Methods: Between January and April 2021, 116 dairy samples (raw milk, traditional cheese, and toof) were collected from Ilam, Iran. Staphylococcus aureus was identified using bacteriological and molecular methods, including PCR targeting femA, mecA, and prophage markers (SGB, SGFa, SGFb). Antibiotic susceptibility was tested via the Kirby-Bauer method, and data were analyzed using SPSS.
Results: S. aureus was detected in 25.9% of samples (30/116), with raw milk showing the highest contamination (57.9%). MRSA, identified by the mecA gene, was present in 6.7% of isolates, and 73.3% exhibited multidrug resistance. Prophages were found in 13.3% of isolates, with SGB linked to β-lactam resistance (p = 0.04). High resistance to doxycycline (87%) and tetracycline (67%) was observed.
Conclusion: The study highlights a significant presence of MRSA and multidrug-resistant S. aureus in Ilam’s dairy products, with prophages contributing to the virulence of these bacteria. Enhanced hygiene and monitoring are crucial for mitigating food safety risks.
1. Cella E, Giovanetti M, Benedetti F, Scarpa F, Johnston C, Borsetti A, et al. Joining forces against antibiotic resistance: The one health solution. Pathogens 2023; 12: 1074.
2. Ifedinezi OV, Nnaji ND, Anumudu CK, Ekwueme CT, Uhegwu CC, Ihenetu FC, et al. Environmental antimicrobial resistance: implications for food safety and public health. Antibiotics (Basel) 2024; 13: 1087.
3. Di Pietro M, Filardo S, Sessa R. Editorial for the special issue "Antibacterial activity of drug-resistant strains". Int J Mol Sci 2024; 25: 1878.
4. Lekshmi M, Ammini P, Kumar S, Varela MF. The food production environment and the development of antimicrobial resistance in human pathogens of animal origin. Microorganisms 2017; 5: 11.
5. Clifford K, Desai D, da Costa CP, Meyer H, Klohe K, Winkler AS, et al. Antimicrobial resistance in livestock and poor-quality veterinary medicines. Bull World Health Organ 2018; 96: 662-664.
6. Hennekinne JA, De Buyser ML, Dragacci S. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev 2012; 36: 815-836.
7. Zhang Z, Liu W, Xu H, Aguilar ZP, Shah NP, Wei H. Propidium monoazide combined with real-time PCR for selective detection of viable Staphylococcus aureus in milk powder and meat products. J Dairy Sci 2015; 98:1625-1633.
8. Klimešová M, Manga I, Nejeschlebová L, Horáček J, Ponížil A, Vondrušková E. Occurrence of Staphylococcus aureus in cattle, sheep, goat, and pig rearing in the Czech Republic. Acta Vet Brno 2017; 86: 3-10.
9. Jackson CR, Davis JA, Barrett JB. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. J Clin Microbiol 2013; 51: 1199-1207.
10. Ou C, Shang D, Yang J, Chen B, Chang J, Jin F, et al. Prevalence of multidrug-resistant Staphylococcus aureus isolates with strong biofilm formation ability among animal-based food in Shanghai. Food Control 2020; 112: 107106.
11. Schnitt A, Tenhagen B. Risk factors for the occurrence of Methicillin-Resistant Staphylococcus aureus in dairy herds: an update. Foodborne Pathog Dis 2020; 17: 585-596.
12. Titouche Y, Hakem A, Houali K, Meheut T, Vingadassalon N, Ruiz-Ripa L, et al. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) ST8 in raw milk and traditional dairy products in the Tizi Ouzou area of Algeria. J Dairy Sci 2019; 102: 6876-6884.
13. 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.
14. 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.
15. Lienen T, Schnitt A, Cuny C, Maurischat S, Tenhagen BA. Phylogenetic tracking of LA-MRSA ST398 intra-farm transmission among animals, humans and the environment on German dairy farms. Microorganisms 2021; 9: 1119.
16. Zhang Z, Wang J, Wang H, Zhang L, Shang W, Li Z, et al. Molecular surveillance of MRSA in raw milk provides insight into MRSA cross species evolution. Microbiol Spectr 2023; 11(4): e0031123.
17. Alkuraythi DM, Alkhulaifi MM. Methicillin-resistant Staphylococcus aureus prevalence in food-producing animals and food products in Saudi Arabia: A review. Vet World 2024; 17: 1753-1764.
18. Khanal S, Boonyayatra S, Awaiwanont N. Prevalence of methicillin-resistant Staphylococcus aureus in dairy farms: A systematic review and meta-analysis. Front Vet Sci 2022; 9: 947154.
19. Al-Ashmawy MA, Sallam KI, Abd-Elghany SM, Elhadidy M, Tamura T. Prevalence, Molecular characterization, and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolated from milk and dairy products. Foodborne Pathog Dis 2016; 13: 156-162.
20. Paterson GK, Morgan FJ, Harrison EM, Peacock SJ, Parkhill J, Zadoks RN, et al. Prevalence and properties of mecC methicillin-resistant Staphylococcus aureus (MRSA) in bovine bulk tank milk in Great Britain. J Antimicrob Chemother 2014; 69: 598-602.
21. Tegegne H, Ejigu E, Woldegiorgis D, Mengistu A. Isolation and antimicrobial resistance patterns of methicillin-resistant Staphylococcus aureus from raw cow's milk in dairy farms of Wolaita Sodo Town, Southwest, Ethiopia. Food Sci Nutr 2024; 12: 4735-4744.
22. Ou Q, Zhou J, Lin D, Bai C, Zhang T, Lin J, et al. A large meta-analysis of the global prevalence rates of S. aureus and MRSA contamination of milk. Crit Rev Food Sci Nutr 2018; 58: 2213-2228.
23. Magaziner SJ, Zeng Z, Chen B, Salmond GP. The Prophages of Citrobacter rodentium represent a conserved family of horizontally acquired mobile genetic elements associated with enteric evolution towards pathogenicity. J Bacteriol 2019; 201(9): e00638-18.
24. Patel PH, Maxwell KL. Prophages provide a rich source of antiphage defense systems. Curr Opin Microbiol 2023; 73: 102321.
25. Varani AM, Monteiro-Vitorello CB, Nakaya HI, Van Sluys MA. The role of prophage in plant-pathogenic bacteria. Annu Rev Phytopathol 2013; 51: 429-451.
26. Vale FF, Roberts RJ, Kobayashi I, Camargo MC, Rabkin CS, HpGP Research Network. Gene content, phage cycle regulation model and prophage inactivation disclosed by prophage genomics in the Helicobacter pylori Genome Project. Gut Microbes 2024; 16: 2379440.
27. Asadulghani MD, Ogura Y, Ooka T, Itoh T, Sawaguchi A, Iguchi A, et al. The defective prophage pool of Escherichia coli O157: Prophage–prophage interactions potentiate horizontal transfer of virulence determinants. PLoS Pathog 2009; 5(5): e1000408.
28. Kondo K, Kawano M, Sugai M. Distribution of antimicrobial resistance and virulence genes within the prophage-associated regions in nosocomial pathogens. mSphere 2021; 6(4): e0045221.
29. Nepal R, Houtak G, Shaghayegh G, Bouras G, Shearwin K, Psaltis AJ, et al. Prophages encoding human immune evasion cluster genes are enriched in Staphylococcus aureus isolated from chronic rhinosinusitis patients with nasal polyps. Microb Genom 2021; 7: 000726.
30. Tavarideh F, Pourahmad F, Nemati M. Diversity and antibacterial activity of endophytic bacteria associated with medicinal plant, Scrophularia striata. Vet Res Forum 2022; 13: 409-415.
31. Adeyemi FM, Oyedara OO, Yusuf-Omoloye NA, Ajigbewu OH, Ndaji OL, Adegbite-Badmus MK, et al. Guardians of resistance and virulence: detection of mec, femA, Van, pvl, hlg and spa genes in methicillin and vancomycin-resistant Staphylococcus aureus from clinical and food samples in Southwestern Nigeria. BMC Microbiol 2024; 24: 498.
32. Kobayashi N, Wu H, Kojima K, Taniguchi K, Urasawa S, Uehara N, et al. Detection of mecA, femA, and femB genes in clinical strains of staphylococci using polymerase chain reaction. Epidemiol Infect 1994; 113: 259-266.
33. Pantůček R, Doškař J, Růžičková V, Kašpárek P, Oráčová E, Kvardová V, et al. Identification of bacteriophage types and their carriage in Staphylococcus aureus. Arch Virol 2004; 149: 1689-1703.
34. CLSI (2022). Performance standards for antimicrobial susceptibility testing. In: CLSI supplement M100. 32nd ed. Clinical and Laboratory Standards Institute, Wayne, PA. https://clsi.org/shop/standards/m100/ (Accessed on 1/17/2024).
35. Dehkordi NV, Rahimi E, Jahromi NZ. 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: 605-613.
36. Lemma F, Alemayehu H, Stringer A, Eguale T. Prevalence and antimicrobial susceptibility profile of Staphylococcus aureus in milk and traditionally processed dairy products in Addis Ababa, Ethiopia. Biomed Res Int 2021; 2021: 5576873.
37. Sadat A, Shata RR, Farag AM, Ramadan H, Alkhedaide A, Soliman MM, et al. Prevalence and characterization of pvl-positive Staphylococcus aureus isolated from raw cow's milk. Toxins (Basel) 2022; 14: 97.
38. Vandendriessche S, Vanderhaeghen W, Soares FV, Hallin M, Catry B, Hermans K, et al. Prevalence, risk factors and genetic diversity of methicillin-resistant Staphylococcus aureus carried by humans and animals across livestock production sectors. J Antimicrob Chemother 2013; 68: 1510-1516.
39. Locatelli C, Cremonesi P, Caprioli A, Carfora V, Ianzano A, Barberio A, et al. Occurrence of methicillin-resistant Staphylococcus aureus in dairy cattle herds, related swine farms, and humans in contact with herds. J Dairy Sci 2017; 100: 608-619.
40. Cortimiglia CE, Bianchini V, Franco A, Caprioli A, Battisti A, Colombo L, et al. Short communication: prevalence of Staphylococcus aureus and methicillin-resistant S. aureus in bulk tank milk from dairy goat farms in Northern Italy. J Dairy Sci 2015; 98: 2307-2311.
41. Algammal AM, Enany ME, El-Tarabili RM, Ghobashy MO, Helmy YA. Prevalence, antimicrobial resistance profiles, virulence and enterotoxins-determinant genes of MRSA isolated from subclinical bovine mastitis in Egypt. Pathogens 2020; 9: 362.
42. Nepal R, Houtak G, Bouras G, Feizi S, Shaghayegh G, Shearwin K, et al. A φSa3int (NM3) prophage domestication in Staphylococcus aureus leads to increased virulence through human immune evasion. MedComm (2020) 2025; 6(8): e70313.
43. Rohmer C, Wolz C. The role of hlb-converting bacteriophages in Staphylococcus aureus host adaption.
Microb Physiol 2021; 31: 109-122.
44. Tran PM, Feiss M, Kinney KJ, Salgado-Pabón W. ϕSa3mw prophage as a molecular regulatory switch of Staphylococcus aureus β-toxin production. J Bacteriol 2019; 201(14): e00766-18.
45. Zhu Z, Wu S, Chen X, Tan W, Zou G, Huang Q, et al. Heterogeneity and transmission of food safety-related enterotoxigenic Staphylococcus aureus in pig abattoirs in Hubei, China. Microbiol Spectr 2023; 11(5): e0191323.
46. Guo H, Pan L, Li L, Lu J, Kwok L, Menghe B, et al. Characterization of antibiotic resistance genes from Lactobacillus isolated from traditional dairy products. J Food Sci 2017; 82: 724-730.
47. Kerek Á, Németh V, Szabó Á, Papp M, Bányai K, Kardos G, et al. Monitoring changes in the antimicrobial-resistance gene set (ARG) of raw milk and dairy products in a cattle farm, from production to consumption. Vet Sci 2024; 11: 265.
48. Adnyana IM, Utomo B, Eljatin DS, Sudaryati NL. One Health approach and zoonotic diseases in Indonesia: Urgency of implementation and challenges. Narra J 2023; 3(3): e257.
49. Da Cunha DT. Improving food safety practices in the foodservice industry. Curr Opin Food Sci 2021; 42: 127-133.
2. Ifedinezi OV, Nnaji ND, Anumudu CK, Ekwueme CT, Uhegwu CC, Ihenetu FC, et al. Environmental antimicrobial resistance: implications for food safety and public health. Antibiotics (Basel) 2024; 13: 1087.
3. Di Pietro M, Filardo S, Sessa R. Editorial for the special issue "Antibacterial activity of drug-resistant strains". Int J Mol Sci 2024; 25: 1878.
4. Lekshmi M, Ammini P, Kumar S, Varela MF. The food production environment and the development of antimicrobial resistance in human pathogens of animal origin. Microorganisms 2017; 5: 11.
5. Clifford K, Desai D, da Costa CP, Meyer H, Klohe K, Winkler AS, et al. Antimicrobial resistance in livestock and poor-quality veterinary medicines. Bull World Health Organ 2018; 96: 662-664.
6. Hennekinne JA, De Buyser ML, Dragacci S. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev 2012; 36: 815-836.
7. Zhang Z, Liu W, Xu H, Aguilar ZP, Shah NP, Wei H. Propidium monoazide combined with real-time PCR for selective detection of viable Staphylococcus aureus in milk powder and meat products. J Dairy Sci 2015; 98:1625-1633.
8. Klimešová M, Manga I, Nejeschlebová L, Horáček J, Ponížil A, Vondrušková E. Occurrence of Staphylococcus aureus in cattle, sheep, goat, and pig rearing in the Czech Republic. Acta Vet Brno 2017; 86: 3-10.
9. Jackson CR, Davis JA, Barrett JB. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. J Clin Microbiol 2013; 51: 1199-1207.
10. Ou C, Shang D, Yang J, Chen B, Chang J, Jin F, et al. Prevalence of multidrug-resistant Staphylococcus aureus isolates with strong biofilm formation ability among animal-based food in Shanghai. Food Control 2020; 112: 107106.
11. Schnitt A, Tenhagen B. Risk factors for the occurrence of Methicillin-Resistant Staphylococcus aureus in dairy herds: an update. Foodborne Pathog Dis 2020; 17: 585-596.
12. Titouche Y, Hakem A, Houali K, Meheut T, Vingadassalon N, Ruiz-Ripa L, et al. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) ST8 in raw milk and traditional dairy products in the Tizi Ouzou area of Algeria. J Dairy Sci 2019; 102: 6876-6884.
13. 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.
14. 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.
15. Lienen T, Schnitt A, Cuny C, Maurischat S, Tenhagen BA. Phylogenetic tracking of LA-MRSA ST398 intra-farm transmission among animals, humans and the environment on German dairy farms. Microorganisms 2021; 9: 1119.
16. Zhang Z, Wang J, Wang H, Zhang L, Shang W, Li Z, et al. Molecular surveillance of MRSA in raw milk provides insight into MRSA cross species evolution. Microbiol Spectr 2023; 11(4): e0031123.
17. Alkuraythi DM, Alkhulaifi MM. Methicillin-resistant Staphylococcus aureus prevalence in food-producing animals and food products in Saudi Arabia: A review. Vet World 2024; 17: 1753-1764.
18. Khanal S, Boonyayatra S, Awaiwanont N. Prevalence of methicillin-resistant Staphylococcus aureus in dairy farms: A systematic review and meta-analysis. Front Vet Sci 2022; 9: 947154.
19. Al-Ashmawy MA, Sallam KI, Abd-Elghany SM, Elhadidy M, Tamura T. Prevalence, Molecular characterization, and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolated from milk and dairy products. Foodborne Pathog Dis 2016; 13: 156-162.
20. Paterson GK, Morgan FJ, Harrison EM, Peacock SJ, Parkhill J, Zadoks RN, et al. Prevalence and properties of mecC methicillin-resistant Staphylococcus aureus (MRSA) in bovine bulk tank milk in Great Britain. J Antimicrob Chemother 2014; 69: 598-602.
21. Tegegne H, Ejigu E, Woldegiorgis D, Mengistu A. Isolation and antimicrobial resistance patterns of methicillin-resistant Staphylococcus aureus from raw cow's milk in dairy farms of Wolaita Sodo Town, Southwest, Ethiopia. Food Sci Nutr 2024; 12: 4735-4744.
22. Ou Q, Zhou J, Lin D, Bai C, Zhang T, Lin J, et al. A large meta-analysis of the global prevalence rates of S. aureus and MRSA contamination of milk. Crit Rev Food Sci Nutr 2018; 58: 2213-2228.
23. Magaziner SJ, Zeng Z, Chen B, Salmond GP. The Prophages of Citrobacter rodentium represent a conserved family of horizontally acquired mobile genetic elements associated with enteric evolution towards pathogenicity. J Bacteriol 2019; 201(9): e00638-18.
24. Patel PH, Maxwell KL. Prophages provide a rich source of antiphage defense systems. Curr Opin Microbiol 2023; 73: 102321.
25. Varani AM, Monteiro-Vitorello CB, Nakaya HI, Van Sluys MA. The role of prophage in plant-pathogenic bacteria. Annu Rev Phytopathol 2013; 51: 429-451.
26. Vale FF, Roberts RJ, Kobayashi I, Camargo MC, Rabkin CS, HpGP Research Network. Gene content, phage cycle regulation model and prophage inactivation disclosed by prophage genomics in the Helicobacter pylori Genome Project. Gut Microbes 2024; 16: 2379440.
27. Asadulghani MD, Ogura Y, Ooka T, Itoh T, Sawaguchi A, Iguchi A, et al. The defective prophage pool of Escherichia coli O157: Prophage–prophage interactions potentiate horizontal transfer of virulence determinants. PLoS Pathog 2009; 5(5): e1000408.
28. Kondo K, Kawano M, Sugai M. Distribution of antimicrobial resistance and virulence genes within the prophage-associated regions in nosocomial pathogens. mSphere 2021; 6(4): e0045221.
29. Nepal R, Houtak G, Shaghayegh G, Bouras G, Shearwin K, Psaltis AJ, et al. Prophages encoding human immune evasion cluster genes are enriched in Staphylococcus aureus isolated from chronic rhinosinusitis patients with nasal polyps. Microb Genom 2021; 7: 000726.
30. Tavarideh F, Pourahmad F, Nemati M. Diversity and antibacterial activity of endophytic bacteria associated with medicinal plant, Scrophularia striata. Vet Res Forum 2022; 13: 409-415.
31. Adeyemi FM, Oyedara OO, Yusuf-Omoloye NA, Ajigbewu OH, Ndaji OL, Adegbite-Badmus MK, et al. Guardians of resistance and virulence: detection of mec, femA, Van, pvl, hlg and spa genes in methicillin and vancomycin-resistant Staphylococcus aureus from clinical and food samples in Southwestern Nigeria. BMC Microbiol 2024; 24: 498.
32. Kobayashi N, Wu H, Kojima K, Taniguchi K, Urasawa S, Uehara N, et al. Detection of mecA, femA, and femB genes in clinical strains of staphylococci using polymerase chain reaction. Epidemiol Infect 1994; 113: 259-266.
33. Pantůček R, Doškař J, Růžičková V, Kašpárek P, Oráčová E, Kvardová V, et al. Identification of bacteriophage types and their carriage in Staphylococcus aureus. Arch Virol 2004; 149: 1689-1703.
34. CLSI (2022). Performance standards for antimicrobial susceptibility testing. In: CLSI supplement M100. 32nd ed. Clinical and Laboratory Standards Institute, Wayne, PA. https://clsi.org/shop/standards/m100/ (Accessed on 1/17/2024).
35. Dehkordi NV, Rahimi E, Jahromi NZ. 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: 605-613.
36. Lemma F, Alemayehu H, Stringer A, Eguale T. Prevalence and antimicrobial susceptibility profile of Staphylococcus aureus in milk and traditionally processed dairy products in Addis Ababa, Ethiopia. Biomed Res Int 2021; 2021: 5576873.
37. Sadat A, Shata RR, Farag AM, Ramadan H, Alkhedaide A, Soliman MM, et al. Prevalence and characterization of pvl-positive Staphylococcus aureus isolated from raw cow's milk. Toxins (Basel) 2022; 14: 97.
38. Vandendriessche S, Vanderhaeghen W, Soares FV, Hallin M, Catry B, Hermans K, et al. Prevalence, risk factors and genetic diversity of methicillin-resistant Staphylococcus aureus carried by humans and animals across livestock production sectors. J Antimicrob Chemother 2013; 68: 1510-1516.
39. Locatelli C, Cremonesi P, Caprioli A, Carfora V, Ianzano A, Barberio A, et al. Occurrence of methicillin-resistant Staphylococcus aureus in dairy cattle herds, related swine farms, and humans in contact with herds. J Dairy Sci 2017; 100: 608-619.
40. Cortimiglia CE, Bianchini V, Franco A, Caprioli A, Battisti A, Colombo L, et al. Short communication: prevalence of Staphylococcus aureus and methicillin-resistant S. aureus in bulk tank milk from dairy goat farms in Northern Italy. J Dairy Sci 2015; 98: 2307-2311.
41. Algammal AM, Enany ME, El-Tarabili RM, Ghobashy MO, Helmy YA. Prevalence, antimicrobial resistance profiles, virulence and enterotoxins-determinant genes of MRSA isolated from subclinical bovine mastitis in Egypt. Pathogens 2020; 9: 362.
42. Nepal R, Houtak G, Bouras G, Feizi S, Shaghayegh G, Shearwin K, et al. A φSa3int (NM3) prophage domestication in Staphylococcus aureus leads to increased virulence through human immune evasion. MedComm (2020) 2025; 6(8): e70313.
43. Rohmer C, Wolz C. The role of hlb-converting bacteriophages in Staphylococcus aureus host adaption.
Microb Physiol 2021; 31: 109-122.
44. Tran PM, Feiss M, Kinney KJ, Salgado-Pabón W. ϕSa3mw prophage as a molecular regulatory switch of Staphylococcus aureus β-toxin production. J Bacteriol 2019; 201(14): e00766-18.
45. Zhu Z, Wu S, Chen X, Tan W, Zou G, Huang Q, et al. Heterogeneity and transmission of food safety-related enterotoxigenic Staphylococcus aureus in pig abattoirs in Hubei, China. Microbiol Spectr 2023; 11(5): e0191323.
46. Guo H, Pan L, Li L, Lu J, Kwok L, Menghe B, et al. Characterization of antibiotic resistance genes from Lactobacillus isolated from traditional dairy products. J Food Sci 2017; 82: 724-730.
47. Kerek Á, Németh V, Szabó Á, Papp M, Bányai K, Kardos G, et al. Monitoring changes in the antimicrobial-resistance gene set (ARG) of raw milk and dairy products in a cattle farm, from production to consumption. Vet Sci 2024; 11: 265.
48. Adnyana IM, Utomo B, Eljatin DS, Sudaryati NL. One Health approach and zoonotic diseases in Indonesia: Urgency of implementation and challenges. Narra J 2023; 3(3): e257.
49. Da Cunha DT. Improving food safety practices in the foodservice industry. Curr Opin Food Sci 2021; 42: 127-133.
| Files | ||
| Issue | Vol 18 No 1 (2026) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v18i1.20934 | |
| Keywords | ||
| Methicillin-resistant Staphylococcus aureus Dairy products Prophages Drug resistance Food safety | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Hashemi AA, Nemati M, Pourahmad F. Prophage typing of Staphylococcus aureus in traditional dairy products of Ilam, Iran. Iran J Microbiol. 2026;18(1):82-90.
