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http://dx.doi.org/10.4014/jmb.1502.02034

Antibiotic Resistance and Virulence Potentials of Shiga Toxin-Producing Escherichia coli Isolates from Raw Meats of Slaughterhouses and Retail Markets in Korea  

Park, Hyun-jung (Ministry of Food and Drug Safety)
Yoon, Jang Won (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University)
Heo, Eun-Jeong (Ministry of Food and Drug Safety)
Ko, Eun-Kyoung (Animal and Plant Quarantine Agency)
Kim, Ki-Yeon (College of Veterinary Medicine, Seoul National University)
Kim, Young-Jo (Ministry of Food and Drug Safety)
Yoon, Hyang-Jin (Animal and Plant Quarantine Agency)
Wee, Sung-Hwan (Animal and Plant Quarantine Agency)
Park, Yong Ho (College of Veterinary Medicine, Seoul National University)
Moon, Jin San (Animal and Plant Quarantine Agency)
Publication Information
Journal of Microbiology and Biotechnology / v.25, no.9, 2015 , pp. 1460-1466 More about this Journal
Abstract
In this study, the prevalence of Shiga toxin-producing Escherichia coli (STEC) was investigated among raw meat or meat products from slaughterhouses and retail markets in South Korea, and their potential for antibiotic resistance and virulence was further analyzed. A total of 912 raw meats, including beef, pork, and chicken, were collected from 2008 to 2009. E. coli strains were frequently isolated in chicken meats (176/233, 75.9%), beef (102/217, 42.3%), and pork (109/235, 39.2%). Putative STEC isolates were further categorized, based on the presence or absence of the Shiga toxin (stx) genes, followed by standard O-serotyping. Polymerase chain reaction assays were used to detect the previously defined virulence genes in STEC, including Shiga toxins 1 and Shiga toxin 2 (stx1 and 2), enterohemolysin (ehxA), intimin (eaeA), STEC autoagglutination adhesion (saa), and subtilase cytotoxin (subAB). All carried both stx1 and eae genes, but none of them had the stx2, saa, or subAB genes. Six (50.0%) STEC isolates possessed the ehxA gene, which is known to be encoded by the 60-megadalton virulence plasmid. Our antibiogram profiling demonstrated that some STEC strains, particularly pork and chicken isolates, displayed a multiple drug-resistance phenotype. RPLA analysis revealed that all the stx1-positive STEC isolates produced Stx1 only at the undetectable level. Altogether, these results imply that the locus of enterocyte and effacement (LEE)-positive strains STEC are predominant among raw meats or meat products from slaughterhouses or retail markets in Korea.
Keywords
Retail meat; Shiga toxin; Stx-producing E. coli; antibiogram; polymerase chain reaction;
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1 Von Muffling T, Smaijlovic M, Nowak B, Sammet K, Bulte M, Klein G. 2007. Preliminary study of certain serotypes, genetic and antimicrobial resistance profiles of verotoxigenic Escherichia coli (VTEC) isolated in Bosnia and Germany from cattle or pigs and their products. Int. J. Food Microbiol. 117: 185-191.   DOI
2 Wang H, Paton JC, Paton AW. 2007. Pathologic changes in mice induced by subtilase cytotoxin, a potent new Escherichia coli AB5 toxin that targets the endoplasmic reticulum. J. Infect. Dis. 196: 1093-1101.   DOI
3 Saei DH, Ahmadi E, Kazemnia A, Ahmadinia M. 2010. Molecular identification and antibiotic susceptibility patterns of Escherichia coli isolates from sheep faeces samples. Comp. Clin. Pathol. 21: 467-473.   DOI
4 Sanchez S, Martnez R, Rey J, Garca A, Blanco J, Blanco M, et al. 2010. Pheno-genotypic characterisation of Escherichia coli O157:H7 isolates from domestic and wild ruminants. Vet. Microbiol. 142: 445-449.   DOI
5 Sasaki Y, Tsujiyama Y, Kusukawa M, Murakaki M, Katayama S, Yamada Y. 2011. Prevalence and characterization of Shiga toxin-producing Escherichia coli 157 and O26 in beef farms. Vet. Microbiol. 150: 140-145.   DOI
6 Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M, Roy L, et al. 2011. Foodborne illness acquired in the United States major pathogens. Emerg. Infect. Dis. 17: 7-15.   DOI
7 Schmidt H, Beutin L, Karch H. 1995. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect. Immun. 63: 1055-1061.
8 Schroeder CM, Zhao C, DebRoy C, Torcolini J, Zhao S, White DG, et al. 2002. Antimicrobial resistance Escherichia coli O157 isolated from humans, cattle, swine, and food. Appl. Eenviron. Microbiol. 68: 576-581.   DOI
9 Sunde M, Norstrom M. 2006. The prevalence of associations between and conjugal transfer of antibiotic resistance genes in Escherichia coli isolated from Norwegian meat and meat products. J. Antimicrob. Chemother. 58: 741-747.   DOI
10 Tozzoli R, Caprioli A, Cappannella S, Michelacci V, Marziano ML, Morabito S. 2010. Production of the subtilase AB5 cytotoxin by Shiga toxin-negative Escherichia coli. J. Clin. Microbiol. 48: 178-183.   DOI
11 Paris A, Bonardi S, Bacci C, Boni E, Salmi F, Bassi L, Brindani F. 2010. Improvement of biomolecular methods for the identification and typing of Escherichia coli O157:H7 isolated from raw meat. Vet. Res. Commun. 34: S145-S148.   DOI
12 Paton AW, Srimanote P, Woodrow MC, Paton JC. 2001. Characterization of Saa, novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shigatoxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 69: 6999-7009.   DOI
13 Pedersen K, Clark L, Andelt WF, Salman MD. 2006. Prevalence of Shiga toxin-producing Escherichia coli and Salmonella enterica in rock pigeons captured in Fort Collins, Colorado. J. Wildl. Dis. 42: 46-55.   DOI
14 Pinaka O, Pournaras S, Mouchtouri V, Plakokefalos E, Katsiaflaka A, Kolokythopoulou F, et al. 2013. Shiga toxinproducing Escherichia coli in Central Greece: prevalence and virulence genes of O157:H7 and non-O157 in animal feces, vegetables, and humans. Eur. J. Clin. Microbiol. Infect. Dis. 32: 1401-1408.   DOI
15 Pradel N, Livrelli V, Champs C, Palcoux JB, Reynaud A, Scheutz F, et al. 2000. Prevalence and characterization of Shiga toxin-producing Escherichia coli isolated from cattle, food, and children during a one-year prospective study in France. J. Clin. Microbiol. 38: 1023-1031.
16 MFDS (Ministry of Food and Drug Safety). Outbreak Food Poisoning Statistic System. Available at http://www.kfda.go.kr/e-stat (accessed 3 August 2012).
17 Rajkhowa S, Sarma DK. 2014. Prevalence and antimicrobial resistance of porcine O157 and non-O157 Shiga toxinproducing Escherichia coli from India. Trop. Anim. Health Prod. 46: 931-937.   DOI
18 Read SC, Gyles CL, Clarke RC, Lior H, McEwen S. 1990. Prevalence of verocytotoxigenic Escherichia coli in ground beef, pork and chicken in Ontario. Epidemiol. Infect. 105: 11-20.   DOI
19 Lee YG, Jang IH, Hwang GI, Rhee SM. 2009. Prevalence and classification of pathogenic Escherichia coli isolated from fresh beef, poultry, and pork in Korea. Int. Food Microbiol. 134: 196-200.   DOI
20 Mohlatlole RP, Madoroba E, Muchadeyi FC, Chimonyo M, Kanengoni T, Dzomba EF. 2013. Virulence profiles of enterotoxigenic, shiga toxin and enteroaggregative Escherichia coli in South African pigs. Trop. Anim. Health Prod. 45: 1399-1405.   DOI
21 Moredo FA, Cappuccio JA, Insarralde L, Perfumo CJ, Quiroga MA, Leotta GA. 2012. Genotypic characterization of toxigenic Escherichia coli isolated from pigs with postweaning diarrhea (PWD) and edema disease (ED). Rev. Argent. Microbiol. 44: 85-88.
22 MFDS (Ministry of Food and Drug Safety). Standards for processing and ingredients specifications of livestock products (MFDS notice 2013-244).
23 Mora A, Blanco EJ, Blanco M, Pilar Alonso M, Dhabi G, Echeita A, et al. 2005. Antimicrobial resistance of Shiga toxin (verotoxin)-producing Escherichia coli O157:H7 and non-O157 strains isolated from humans, cattle, sheep and food in Spain. Res. Microbiol. 156: 793-806.   DOI
24 Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142-201.
25 Ghanbarpour R, Kiani M. 2013. Characterization of non-O157 Shiga toxin-producing Escherichia coli isolates from healthy fat-tailed sheep in southeastern of Iran. Trop. Anim. Health Prod. 45: 641-648.   DOI
26 Pacheco AR, Sperandio V. 2012. Shiga toxin in enterohemorrhagic E. coli: regulation and novel anti-virulence strategies. Front. Cell Infect. Microbiol. 2: 81.   DOI
27 Park SH, Kim SH, Seo JJ, Kee HY, Kim MJ, Seo KW, et al. 2006. An outbreak of inapparent non-O157 enterohemorrhagic Escherihia coli infection. Kor. J. Med. 70: 495-504.
28 Gautam R, Bani-Yaghoub M, Neill WH, Döpfer D, Kaspar C, Ivanek R. 2011. Modeling the effect of seasonal variation in ambient temperature on the transmission dynamics of a pathogen with a free-living stage: example of Escherichia coli O157:H7 in a dairy herd. Prev. Vet. Med. 102: 10-21.   DOI
29 Grant MA, Hedberg C, Johnson R, Harris J, Logue CM, Meng J, Sofos N, Dickson JS. 2011. The significance of non-O157 Shiga toxin-producing Escherichia coli in food. Food Protect. Trends 31: 33-56.
30 Growther L, Lullu PK, Sukirtha K, Niren Andrew S. 2013. Biotyping, molecular characterization and screening for antibacterial phytochemicals against Shiga toxin producing E. coli from cattle. Arch. Appl. Sci. Res. 5: 178-182.
31 Gyles CL. 2007. Shiga toxin-producing Escherichia coli: an overview. J. Anim. Sci. 5: E45-E62.   DOI
32 Helmy OM, Ragab YM, Hussein M. 2013. Multiplex polymerase chain reaction (PCR) for the detection of diarrheagenic Escherichia coli and Shigella directly from stool. Afr. J. Microbiol. Res. 7: 4368-4372.
33 Coombes BK, Gilmour MW, Goodman CD. 2011. The evolution of virulence in non-O157 Shiga toxin-producing Escherichia coli. Frontiers Microbiol. 2: 1-3.   DOI
34 Jenkins C, Perry NT, Cheasty T, Shaw DJ, Frankel G, Dougan G, et al. 2003. Distribution of the saa gene in strains of Shiga toxin-producing Escherichia coli of human and bovine origins. J. Clin. Microbiol. 41: 1775-1778.   DOI
35 Kaufmann M, Zweifel C, Blanco M, Blanco JE, Blanco J, Beutin L, Stephan R. 2006. Escherichia coli O157 and non-O157 Shiga toxin-producing Escherichia coli in fecal samples of finished pigs at slaughter in Switzerland. J. Food. Prot. 9: 260-266.
36 Brooks TJ, Sowers EG, Wells JG, Greene KD, Griffin PM, Hoekstra RM, Strockbine NA. 2005. Non-O157 Shiga toxin–producing Escherichia coli infections in the United States, 1983–2002. J. Infect. Dis. 192: 1422-1449.   DOI
37 Choi SK, Lee MH, Lee BH, Jung JY, Choi C. 2010. Virulence factor profiles of Escherichia coli isolated from pork and chicken meats obtained from retail markets. Kor. J. Food Sci. Anim. Resour. 30: 148-153.   DOI
38 CLSI. 2008. Performance standards for antimicrobial disk and dilution susceptibility tests or bacteria isolated from animals; Approved Standard, 3rd Ed. Vol. 28. Clinical and Laboratory Standards Institute, Wayne, PA, USA.
39 Díaz-Sánchez S, Sánchez S, Herrera-León S, Porrero C, Blanco J, Dahbi, Blanco JE, et al. 2013. Prevalence of Shiga toxinproducing Escherichia coli, Salmonella spp. and Campylobacter spp. in large game animals intended for consumption: relationship with management practices and livestock influence. Vet. Microbiol. 163: 274-281.   DOI
40 EFSA. 2007. European Food Safety Authority. Scientific opinion of the panel on biological hazards on a request from EFSA on monitoring of verotoxigenic Escherichia coli. EFSA J. 579: 1-61.
41 Evans J, Wilson A, Willshaw GA, Cheasty T, Tompkins DS, Wheeler JG, Smith HR. 2002. Vero cytotoxin-producing Escherichia coli in a study of infectious intestinal disease in England. Clin. Microbiol. Infect. 8: 183-186.   DOI
42 Fernández D, Sanz ME, Parma AE, Padola NL. 2012. Characterization of Shiga toxin producing Escherichia coli isolated from newborn, milk-fed, and growing calves in Argentina. J. Dairy Sci. 95: 5340-5343.   DOI
43 Ayala CO, Moreno RAC, Martinez MB, Castro PAF, Bando SY. 2012. Determination of flagellar types by PCR-RFLP analysis of enteropathogenic Escherichia coli (EPEC) and Shiga toxin-producing E. coli (STEC) strains isolated from animals in São Paulo, Brazil. Res. Vet. Sci. 92: 18-23.   DOI
44 Bettelheim KA. 2007. The non-O157 Shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit. Rev. Microbiol. 33: 67-87.   DOI
45 Beutin L, Miko A, Krause G, Pries K, Haby S, Steege K, Albrecht N. 2007. Identification of human-pathogenic strains of Shiga toxin-producing Escherichia coli from food by a combination of serotyping and molecular typing of Shiga toxin genes. Appl. Environ. Microbiol. 73: 4769-4775.   DOI
46 USDA. 2012. United States Department of Agriculture. Shiga toxin-producing Escherichia coli in certain raw beef products. Docket No. FSIS-2010-0023. Federal Register 77: 9888-9889.
47 USDA. 2011. United States Department of Agriculture. Draft risk profile for pathogenicon-O157 Shiga toxin-producing Escherichia coli (non-O157 STEC). Available at http://www.fsis.usda.gov/PDF/Non_O157_STEC_Risk_Profile.pdf (Accessed 13-April-2012).