Profiles of coagulase-positive and -negative staphylococci in retail pork: prevalence, antimicrobial resistance, enterotoxigenicity, and virulence factors
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Objective: The present study aimed to investigate the occurrence and species of coagulasepositive staphylococci (CoPS) and coagulase-negative staphylococci (CoNS) in retail pork meat samples collected during nationwide monitoring. The staphylococcal isolates were characterized for antimicrobial and zinc chloride resistance and enterotoxigenic potential.Methods: A total of 260 pre-packaged pork meat samples were collected from 35 retail markets in 8 provinces in Korea for isolation of staphylococci. Antimicrobial and zinc chloride resistance phenotypes, and genes associated with the resistance phenotypes were determined on the isolates. Furthermore, the presence and distribution of 19 staphylococcal enterotoxin (SE) genes and enterotoxin-like genes among the pork-associated staphylococci were determined by multiplex polymerase chain reaction-based assays using the specific primer sets.Results: A total of 29 staphylococcal strains (29/260, 11.1%) were isolated from samples of retail pork meat, 24 (83%) of which were CoNS. The four CoNS species identified were <i>S. saprophyticus</i> (n = 16, 55%), <i>S. sciuri</i> (n = 3, 10%), <i>S. warneri</i> (n = 3, 10%), and <i>S. epidermidis</i> (n = 2, 7%). Among the 29 isolates, four methicillin-resistant CoNS (MR-CoNS; three <i>S. sciuri</i> and one <i>S. epidermidis</i>) and one methicillin-resistant CoPS (MR-CoPS; one <i>S. aureus</i>) were identified. In addition, a relatively high level of tetracycline (TET) resistance (52%) was confirmed in CoNS, along with a predominant distribution of <i>tet</i>(K). The most prevalent SEs were <i>sep</i> (45%), and <i>sen</i> (28%), which were carried by 81% of S. saprophyticus.Conclusion: These findings suggest that CoNS, especially <i>S. saprophyticus</i> strains, in raw pork meat could be a potential risk factor for staphylococcal food poisoning (SFP), and therefore, requires further investigation to elucidate the role of SEls in SFP and virulence of the pathogen. Our results also suggest that CoNS from raw pork meat may act as a source for transmission of antimicrobial resistance genes such as staphylococcal cassette chromosome <i>mec</i> and <i>tet</i>(K).
Abstract
Objective: The present study aimed to investigate the occurrence and species of coagulasepositive staphylococci (CoPS) and coagulase-negative staphylococci (CoNS) in retail pork meat samples collected during nationwide monitoring. The staphylococcal isolates were characterized for antimicrobial and zinc chloride resistance and enterotoxigenic potential. Methods: A total of 260 pre-packaged pork meat samples were collected from 35 retail markets in 8 provinces in Korea for isolation of staphylococci. Antimicrobial and zinc chloride resistance phenotypes, and genes associated with the resistance phenotypes were determined on the isolates. Furthermore, the presence and distribution of 19 staphylococcal enterotoxin (SE) genes and enterotoxin-like genes among the pork-associated staphylococci were determined by multiplex polymerase chain reaction-based assays using the specific primer sets. Results: A total of 29 staphylococcal strains (29/260, 11.1%) were isolated from samples of retail pork meat, 24 (83%) of which were CoNS. The four CoNS species identified were S. saprophyticus (n = 16, 55%), S. sciuri (n = 3, 10%), S. warneri (n = 3, 10%), and S. epidermidis (n = 2, 7%). Among the 29 isolates, four methicillin-resistant CoNS (MR-CoNS; three S. sciuri and one S. epidermidis) and one methicillin-resistant CoPS (MR-CoPS; one S. aureus) were identified. In addition, a relatively high level of tetracycline (TET) resistance (52%) was confirmed in CoNS, along with a predominant distribution of tet(K). The most prevalent SEs were sep (45%), and sen (28%), which were carried by 81% of S. saprophyticus. Conclusion: These findings suggest that CoNS, especially S. saprophyticus strains, in raw pork meat could be a potential risk factor for staphylococcal food poisoning (SFP), and therefore, requires further investigation to elucidate the role of SEls in SFP and virulence of the pathogen. Our results also suggest that CoNS from raw pork meat may act as a source for transmission of antimicrobial resistance genes such as staphylococcal cassette chromosome mec and tet(K).
참고문헌 (36)
- Li H, "Antimicrobial resistance and virulence gene profiles of methicillin-resistant and-susceptible Staphylococcus aureus from food products in Denmark", Front Microbiol, 10, pp.2681~ (2019)[DOI]
- Fisher EL, "Basis of virulence in enterotoxin-mediated staphylococcal food poisoning", Front Microbiol, 9, pp.436~ (2018)[DOI]
- Pyzik E, "Detection of antibiotic resistance and classical enterotoxin genes in coagulase-negative staphylococci isolated from poultry in Poland", J Vet Res, 63, pp.183~190 (2019)[DOI]
- Fijalkowski K, "Staphylococci isolated from ready-to-eat meat-identification, antibiotic resistance and toxin gene profile", Int J Food Microbiol, 238, pp.113~120 (2016)[DOI]
- Vanderhaeghen W, "Species and staphylococcal cassette chromosome mec(SCCmec)diversity among methicillin-resistant non-Staphylococcus aureus staphylococci isolated from pigs", Vet Microbiol, 158, pp.123~128 (2012)[DOI]
- Wendlandt S, "Multidrug resistance genes in staphylococci from animals that confer resistance to critically and highly important antimicrobial agents in human medicine", Trends Microbiol, 23, pp.44~54 (2015)[DOI]
- Seung Hyun Back, "Livestock-Associated Methicillin-Resistant Staphylococcus aureus in Korea: Antimicrobial Resistance and Molecular Characteristics of LA-MRSA Strains Isolated from Pigs, Pig Farmers, and Farm Environment", Journal of Veterinary Science, 21(1), pp.0~0 (2020), 대한수의학회[DOI]
- Price LB, "Staphylococcus aureus CC398 : host adaptation and emergence of methicillin resistance in livestock", mBio, 3, pp.e00305~e00311 (2012)[DOI]
- 엄홍식, "Prevalence and Characteristics of Livestock-associated Methicillin-Susceptible Staphylococcus aureus in the Pork Production Chain in Korea", Journal of Veterinary Science, 20(6), pp.1~11 (2019), 대한수의학회[DOI]
- Hau SJ, "Zinc resistance within swine-associated methicillin-resistant Staphylococcus aureus isolates in the United States is associated with multilocus sequence type lineage", Appl Environ Microbiol, 83, pp.e00756-17~ (2017)[DOI]
- Kondo Y, "Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment : rapid identification system for mec, ccr, and major differences in junkyard regions", Antimicrob Agents Chemother, 51, pp.264~274 (2007)[DOI]
- Ng LK, "Multiplex PCR for the detection of tetracycline resistant genes", Mol Cell Probes, 15, pp.209~215 (2001)[DOI]
- Clyne M, "Production of gamma-hemolysin and lack of production of alpha-hemolysin by Staphylococcus aureus strains associated with toxic shock syndrome", J Clin Microbiol, 26, pp.535~539 (1988)[DOI]
- 이희수, "Characterization of the Biodiversity of the Spoilage Microbiota in Chicken Meat Using Next Generation Sequencing and Culture Dependent Approach", 한국축산식품학회지, 37(4), pp.535~541 (2017), 한국축산식품학회
- Park JY, "Detection of classical and newly described staphylococcal superantigen genes in coagulasenegative staphylococci isolated from bovine intramammary infections", Vet Microbiol, 147, pp.149~154 (2011)[DOI]
- Aarestrup FM, "Decreased susceptibility to zinc chloride is associated with methicillin resistant Staphylococcus aureus CC398 in Danish swine", Vet Microbiol, 142, pp.455~457 (2010)[DOI]
- Cavaco LM, "Zinc resistance of Staphylococcus aureus of animal origin is strongly associated with methicillin resistance", Vet Microbiol, 150, pp.344~348 (2011)[DOI]
- Mama OM, "High diversity of coagulase negative staphylococci species in wild boars, with low antimicrobial resistance rates but detection of relevant resistance genes", Comp Immunol Microbiol Infect Dis, 64, pp.125~129 (2019)[DOI]
- Igbinosa EO, "Prevalence of methicillin-resistant Staphylococcus aureus and other Staphylococcus species in raw meat samples intended for human consumption in Benin city, Nigeria : implications for public health", Int J Environ Res Public Health, 13, pp.949~ (2016)[DOI]
- O'Brien AM, "MRSA in conventional and alternative retail pork products", PLoS One, 7, pp.e30092~ (2012)[DOI]
- Wu S, "Staphylococcus aureus isolated from retail meat and meat products in China : incidence, antibiotic resistance and genetic diversity", Front Microbiol, 9, pp.2767~ (2018)[DOI]
- Tulinski P, "Methicillin-resistant coagulase-negative staphylococci on pig farms as a reservoir of heterogeneous staphylococcal cassette chromosome mec elements", Appl Environ Microbiol, 78, pp.299~304 (2012)[DOI]
- de Freitas Guimaraes F, "Enterotoxin genes in coagulase-negative and coagulase-positive staphylococci isolated from bovine milk", J Dairy Sci, 96, pp.2866~2872 (2013)[DOI]
- Rolo J, "Evolutionary origin of the staphylococcal cassette chromosome mec(SCCmec)", Antimicrob Agents Chemother, 61, pp.e02302~e02316 (2017)[DOI]
- Wang YT, "Distribution of antibiotic resistance genes among Staphylococcus species isolated from ready-to-eat foods", J Food Drug Anal, 27, pp.841~848 (2019)[DOI]
- Abdalrahman LS, "Staphylococcus aureus is more prevalent in retail beef livers than in pork and other beef cuts", Pathogens, 4, pp.182~198 (2015)[DOI]
- Li L, "Nasal carriage of methicillin-resistant coagulase-negative staphylococci in healthy humans is associated with occupational pig contact in a dose-response manner", Vet Microbiol, 208, pp.231~238 (2017)[DOI]
- Argudin MA, "Heavy metal and disinfectant resistance genes among livestock-associated methicillin-resistant Staphylococcus aureus isolates", Vet Microbiol, 191, pp.88~95 (2016)[DOI]
- 이행호, "Occurrence and Characteristics of Methicillin- Resistant and -Susceptible Staphylococcus aureus Isolated from the Beef Production Chain in Korea", 한국축산식품학회지, 40(3), pp.401~414 (2020), 한국축산식품학회[DOI]
- Rajeshwari Nair, "Resistance to zinc and cadmium in Staphylococcus aureus of human and animal origin", Infection Control & Hospital Epidemiology, 35(S3), pp.S32~S39 (2014), Cambridge University Press (CUP)[DOI]
- Slifierz MJ, "Zinc-resistance gene czrC identified in methicillin-resistant Staphylococcus hyicus isolated from pigs with exudative epidermitis", Can Vet J, 55, pp.489~490 (2014)
- Argudin MA, "Dissemination of metal resistance genes among animal methicillin-resistant coagulase-negative staphylococci", Res Vet Sci, 105, pp.192~194 (2016)[DOI]
- de Lourdes RS da Cunha M, "Detection of enterotoxin and toxic shock syndrome toxin 1 genes in Staphylococcus, with emphasis on coagulase-negative staphylococci", Microbiol Immunol, 51, pp.381~390 (2007)[DOI]
- Schelin J, "The formation of Staphylococcus aureus enterotoxin in food environments and advances in risk assessment", Virulence, 2, pp.580~592 (2011)[DOI]
- Czop JK, "Staphylococcal enterotoxin synthesis during the exponential, transitional, and stationary growth phases", Infect Immun, 9, pp.229~235 (1974)[DOI]
- Wang G, "Evaluation of the spoilage potential of bacteria isolated from chilled chicken in vitro and in situ", Food Microbiol, 63, pp.139~146 (2017)[DOI]
