Restricted accessResearch articleFirst published online 2015-05
Molecular Characterization,Antibiotic Resistance,and Virulence Factors of Methicillin-Resistant Staphylococcus aureus Strains Isolated from Imported and Domestic Meat in Korea
During a nationwide surveillance in Korea, 13 methicillin-resistant Staphylococcus aureus (MRSA) strains were isolated from imported and domestic meat between 2009 and 2011. The predominant MRSA genotype was SCCmec type V, and only two agr types (I and II) were found. Unexpectedly, sequence type ST72 comprised more than 50% of the isolates; this is the first instance of type ST72 in food from Canada. Two Spanish pork isolates were ST398, which caused human disease in Europe, and they carried leukotoxin genes, lukS, lukF, and lukE-lukD. Furthermore, P71 and P6 harbored all of the known leukocidin genes, lukS-lukF-lukE-lukD-lukM. Our collected MRSA strains were multidrug resistant with various antimicrobial and heavy-metal resistance genes. Toxin genes that are commonly found in clinical MRSA also were detected in our meat strains. One MRSA strain exhibited an uncommon type of enterotoxin, sec-see-seg-sei-sel-sem-sen-seo-sep. Plasmids (1.5–15.0 kb) were found in 12 of the 13 MRSA isolates. Repetitive sequence-based polymerase chain reaction of the genomic DNA showed 3 clusters with 95% similarity. The presence of multidrug-resistant and toxigenic MRSA in meat products suggests that comprehensive surveillance should be continued for imported meats in Korea.
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References
1.
BarrettJF. MRSA: Status and prospects for therapy? An evaluation of key papers on the topic of MRSA and antibiotic resistance. Expert Opin Ther Targets, 2004; 8:515–519.
2.
BhatM, DumortierC, TaylorBS, et al.Staphylococcus aureus ST398, New York City and Dominican Republic. Emerg Infect Dis, 2009; 15:285–287.
3.
BoostMV, HoJ, GuardabassiL, O'DonoghueMM. High methicillin-resistant Staphylococcus aureus carriage in intensive pig farms in southern China. Vet Rec, 2012; 171:156, 1–2.
4.
CampbellSJ, DeshmukhHS, NelsonCL, et al.Genotypic characteristics of Staphylococcus aureus isolates from a multinational trial of complicated skin and skin structure infections. J Clin Microbiol, 2008; 46:678–684.
5.
CavacoLM, HasmanH, AarestrupFM. Zinc resistance of Staphylococcus aureus of animal origin is strongly associated with methicillin resistance. Vet Microbiol, 2011; 150:344–348.
6.
CavacoLM, HasmanH, SteggerM, et al.Cloning and occurrence of czrC, a gene conferring cadmium and zinc resistance in methicillin-resistant Staphylococcus aureus CC398 isolates. Antimicrob Agents Chemother, 2010; 54:3605–3608.
7.
ChurchDL, ChowBL, LloydT, GregsonDB. Comparison of automated repetitive-sequence-based polymerase chain reaction and spa typing versus pulsed-field gel electrophoresis for molecular typing of methicillin-resistant Staphylococcus aureus. Diagn Microbiol Infect Dis, 2011; 69:30–37.
8.
[CLSI] Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. In: 17th Informational Supplement, Volume 27. Wayne, PA: CLSI, 2007, pp. M100–S17.
9.
de BoerE, Zwartkruis-NahuisJT, WitB, et al.Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol, 2009; 134:52–56.
10.
DeLeoFR, DiepBA, OttoM. Host defense and pathogenesis in Staphylococcus aureus infections. Infect Dis Clin North Am, 2009; 23:17–34.
11.
DiepBA, GillSR, ChangRF, et al.Complete genome sequence of USA300, an epidemic clone of community-acquired methicillin-resistant Staphylococcus aureus. Lancet, 2006; 367:731–739.
EllingtonMJ, YearwoodL, GannerM, EastC, KearnsAM. Distribution of the ACME-arcA gene among methicillin-resistant Staphylococcus aureus from England and Wales. J Antimicrob Chemother, 2008; 61:73–77.
14.
EnrightMC, DayNP, DaviesCE, PeacockSJ, SprattBG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol, 2000; 38:1008–1015.
15.
EscobarJA, Marquez-OrtizRA, Alvarez-OlmosMI, et al.Detection of a new community genotype methicillin-resistant Staphylococcus aureus clone that is unrelated to the USA300 clone and that causes pediatric infections in Colombia. J Clin Microbiol, 2013; 51:661–664.
16.
[EFSA] European Food Safety Authority. Analysis of the baseline survey on the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU, Part A: MRSA prevalence estimates. EFSA J, 2009; 7:1376.
17.
GoldingGR, BrydenL, LevettPN, et al.Livestock-associated methicillin-resistant Staphylococcus aureus sequence type 398 in humans, Canada. Emerg Infect Dis, 2010; 16:587–594.
18.
HarmsenD, ClausH, WitteW, et al.Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol, 2003; 41:5442–5448.
19.
HauschildT, SachaP, WieczorekP, ZalewskaM, KaczynskaK, TryniszewskaE. Aminoglycosides resistance in clinical isolates of Staphylococcus aureus from a University Hospital in Bialystok, Poland. Folia Histochem Cytobiol, 2008; 46:225–228.
20.
HennekinneJA, De BuyserML, DragacciS. Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation. FEMS Microbiol Rev, 2012; 36:815–836.
21.
InjacR, MlinaricA, Djorjevic-MilicV, Karljikovic-RajicK, StrukeljB. Optimal conditions for determination of zinc bacitracin, polymyxin B, oxytetracycline and sulfacetamide in animal feed by micellar electrokinetic capillary chromatography. Food Additives Contamin Part A Chem Anal Control Exposure Risk Assess, 2008; 25:424–431.
22.
JacksonCR, DavisJA, BarrettJB. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. J Clin Microbiol, 2013; 51:1199–1207.
23.
JarraudS, MougelC, ThioulouseJ, et al.Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun, 2002; 70:631–641.
24.
KhannaT, FriendshipR, DeweyC, WeeseJS. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Microbiol, 2008; 128:298–303.
25.
KumarR, YadavBR, SinghRS. Genetic determinants of antibiotic resistance in Staphylococcus aureus isolates from milk of mastitic crossbred cattle. Curr Microbiol, 2010; 60:379–386.
26.
LeeHC, KimEH, ChoHS, LeeCH, KimKD, JungBC. Detection of mecA, blaZ and aac(6′)-aph(2) gene of staphylococci by PCR. Korean J Clin Pathol, 2001; 21:505–511.
27.
LimKT, HanifahYA, Mohd YusofMY, ThongKL. Investigation of toxin genes among methicillin-resistant Staphylococcus aureus strains isolated from a tertiary hospital in Malaysia. Trop Biomed, 2012; 29:212–219.
28.
LouieL, GoodfellowJ, MathieuP, GlattA, LouieM, SimorAE. Rapid detection of methicillin-resistant staphylococci from blood culture bottles by using a multiplex PCR assay. J Clin Microbiol, 2002; 40:2786–2790.
29.
LowyFD. Staphylococcus aureus infections. N Engl J Med, 1998; 339:520–532.
30.
MassiddaO, MingoiaM, FaddaD, WhalenMB, MontanariMP, VaraldoPE. Analysis of the beta-lactamase plasmid of borderline methicillin-susceptible Staphylococcus aureus: Focus on bla complex genes and cadmium resistance determinants cadD and cadX. Plasmid, 2006; 55:114–127.
31.
MonacoM, PedroniP, SanchiniA, BonominiA, IndelicatoA, PantostiA. Livestock-associated methicillin-resistant Staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming. BMC Infect Dis, 2013; 13:258.
32.
NoguchiN, TamuraM, NaruiK, WakasugiK, SasatsuM. Frequency and genetic characterization of multidrug-resistant mutants of Staphylococcus aureus after selection with individual antiseptics and fluoroquinolones. Biol Pharm Bull, 2002; 25:1129–1132.
33.
RosdahlVT, RosendalK. Correlation of penicillinase production with phage type and susceptibility to antibiotics and heavy metals in Staphylococcus aureus. J Med Microbiol, 1983; 16:391–399.
34.
SatorresSE, AlcarazLE. Prevalence of icaA and icaD genes in Staphylococcus aureus and Staphylococcus epidermidis strains isolated from patients and hospital staff. Central Eur J Public Health, 2007; 15:87–90.
35.
SchitoGC. The importance of the development of antibiotic resistance in Staphylococcus aureus. Clin Microbiol Infect, 2006; 12(Suppl 1):3–8.
36.
SchmitzFJ, JonesME, HofmannB, et al.Characterization of grlA, grlB, gyrA, and gyrB mutations in 116 unrelated isolates of Staphylococcus aureus and effects of mutations on ciprofloxacin MIC. Antimicrob Agents Chemother, 1998; 42:1249–1252.
37.
SchmitzFJ, KreyA, SadurskiR, et al.Resistance to tetracycline and distribution of tetracycline resistance genes in European Staphylococcus aureus isolates. J Antimicrob Chemother, 2001; 47:239–240.
38.
SchuenckRP, NouerSA, Winter CdeO, et al.Polyclonal presence of non-multiresistant methicillin-resistant Staphylococcus aureus isolates carrying SCCmec IV in health care-associated infections in a hospital in Rio de Janeiro, Brazil. Diagn Microbiol Infect Dis, 2009; 64:434–441.
39.
ShidaH, HwangSH. Meat demand in South Korea. J Agr Appl Econ, 2007; 39:47–60.
40.
ShuklaSK, KarowME, BradyJM, et al.Virulence genes and genotypic associations in nasal carriage, community-associated methicillin-susceptible and methicillin-resistant USA400 Staphylococcus aureus isolates. J Clin Microbiol, 2010; 48:3582–3592.
41.
StrommengerB, KehrenbergC, KettlitzC, et al.Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates. J Antimicrob Chemother, 2006; 57:461–465.
42.
TakahashiH, KikuchiT, ShojiS, et al.Characterization of gyrA, gyrB, grlA and grlB mutations in fluoroquinolone-resistant clinical isolates of Staphylococcus aureus. J Antimicrob Chemother, 1998; 41:49–57.
43.
TakahataM, YonezawaM, KuroseS, et al.Mutations in the gyrA and grlA genes of quinolone-resistant clinical isolates of methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother, 1996; 38:543–546.
44.
TakanoT, HiguchiW, ZaraketH, et al.Novel characteristics of community-acquired methicillin-resistant Staphylococcus aureus strains belonging to multilocus sequence type 59 in Taiwan. Antimicrob Agents Chemother, 2008; 52:837–845.
45.
TrzcinskiK, CooperBS, HryniewiczW, DowsonCG. Expression of resistance to tetracyclines in strains of methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother, 2000; 45:763–770.
46.
VancraeynestD, HermansK, HaesebrouckF. Genotypic and phenotypic screening of high and low virulence Staphylococcus aureus isolates from rabbits for biofilm formation and MSCRAMMs. Vet Microbiol, 2004; 103:241–247.
47.
WatersAE, Contente-CuomoT, BuchhagenJ, et al.Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin Infect Dis, 2011; 52:1227–1230.
48.
WeeseJS, AveryBP, Reid-SmithRJ. Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products. Lett Appl Microbiol, 2010a;51:338–342.
49.
WeeseJS, Reid-SmithR, RousseauJ, AveryB. Methicillin-resistant Staphylococcus aureus (MRSA) contamination of retail pork. Can Vet J Rev Vet Canadienne, 2010b;51:749–752.
50.
ZhangK, McClureJA, ElsayedS, LouieT, ConlyJM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol, 2005; 43:5026–5033.
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