Journal of Microbiology and Biotechnology
The Korean Society for Microbiology and Biotechnology publishes the Journal of Microbiology and Biotechnology.

2015 ; Vol.25-9: 1460~1466

AuthorHyun-jung Park, Jang Won Yoon, Eun-Jeong Heo, Eun-Kyoung Ko, Ki-Yeon Kim, Young-Jo Kim, Hyang-Jin Yoon, Sung-Hwan Wee, Yong Ho Park, Jin San Moon
Place of dutyMinistry of Food and Drug Safety, Cheongwon 363-951, Republic of Korea
TitleAntibiotic Resistance and Virulence Potentials of Shiga Toxin-Producing Escherichia coli Isolates from Raw Meats of Slaughterhouses and Retail Markets in Korea
PublicationInfo J. Microbiol. Biotechnol.2015 ; Vol.25-9
AbstractIn 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.
Full-Text
Key_wordRetail meat, Shiga toxin, Stx-producing E. coli, Antibiogram, polymerase chain reaction
References
  1. 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.
    Pubmed CrossRef
  2. Bettelheim KA. 2007. The non-O157 Shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit. Rev. Microbiol. 33: 67-87.
    Pubmed CrossRef
  3. 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.
    Pubmed CrossRef Pubmed Central
  4. 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.
    Pubmed CrossRef
  5. Coombes BK, Gilmour MW, Goodman CD. 2011. The evolution of virulence in non-O157 Shiga toxin-producing Escherichia coli. Frontiers Microbiol. 2: 1-3.
    Pubmed CrossRef Pubmed Central
  6. 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.
    CrossRef
  7. 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.
  8. 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.
    Pubmed CrossRef
  9. 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.
  10. 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.
    Pubmed CrossRef
  11. 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.
    Pubmed CrossRef
  12. 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.
    Pubmed CrossRef
  13. Ghanbarpour R, Kiani M. 2013. Characterization of nonO157 Shiga toxin-producing Escherichia coli isolates from healthy fat-tailed sheep in southeastern of Iran. Trop. Anim. Health Prod. 45: 641-648.
    Pubmed CrossRef
  14. Grant MA, Hedberg C, Johnson R, Harris J, Logue CM, Meng J , Sofos N, Dickson JS. 2 011. T he s ignificance of nonO157 Shiga toxin-producing Escherichia coli in food. Food Protect. Trends 31: 33-56.
  15. 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.
  16. Gyles CL. 2007. Shiga toxin-producing Escherichia coli: an overview. J. Anim. Sci. 5: E45-E62.
    Pubmed CrossRef
  17. 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.
  18. 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.
    Pubmed CrossRef Pubmed Central
  19. Kaufmann M, Zweifel C, Blanco M, Blanco JE, Blanco J, Beutin L, Stephan R. 2006. Escherichia coli O157 and nonO157 Shiga toxin-producing Escherichia coli in fecal samples of finished pigs at slaughter in Switzerland. J. Food. Prot. 9:260-266.
  20. 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.
    Pubmed CrossRef
  21. 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).
  22. 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: 13991405.
    Pubmed CrossRef
  23. 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.
    Pubmed
  24. MFDS (Ministry of Food and Drug Safety). Standards for processing and ingredients specifications of livestock products (MFDS notice 2013-244).
  25. 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 nonO157 strains isolated from humans, cattle, sheep and food in Spain. Res. Microbiol. 156: 793-806.
    Pubmed CrossRef
  26. Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142-201.
    Pubmed Pubmed Central
  27. Pacheco AR, Sperandio V. 2012. Shiga toxin in enterohemorrhagic E. coli: regulation and novel anti-virulence strategies. Front. Cell Infect. Microbiol. 2: 81.
    Pubmed CrossRef Pubmed Central
  28. 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.
  29. 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.
    Pubmed CrossRef
  30. 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.
    Pubmed CrossRef Pubmed Central
  31. 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.
    Pubmed CrossRef
  32. 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.
    Pubmed CrossRef
  33. 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.
    Pubmed Pubmed Central
  34. 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.
    Pubmed CrossRef
  35. 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.
    Pubmed CrossRef Pubmed Central
  36. 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.
    CrossRef
  37. Sanchez S, Mart nez R, Rey J, Garc a 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.
    Pubmed CrossRef
  38. 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.
    Pubmed CrossRef
  39. 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.
    Pubmed CrossRef Pubmed Central
  40. 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.
    Pubmed Pubmed Central
  41. 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.
    Pubmed CrossRef Pubmed Central
  42. 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.
    Pubmed CrossRef
  43. 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.
    Pubmed CrossRef Pubmed Central
  44. USDA. 2011. United States Department of Agriculture. Draft risk profile for pathogenicon-O157 Shiga toxin-producing Escherichia coli ( non-O157 S T EC). A vailable a t http://www.fsis.usda.gov/PDF/Non_O157_STEC_Risk_Profile.pdf (Accessed13-April-2012).
  45. 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.
  46. 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.
    Pubmed CrossRef
  47. 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.
    Pubmed CrossRef



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