Annals of Microbiology

, Volume 65, Issue 4, pp 1993–1999 | Cite as

Prevalence and characterization of Escherichia coli O157 and O157:H7 in retail fresh raw meat in South China

  • Shuhong Zhang
  • Xuemei Zhu
  • Qingping WuEmail author
  • Jumei Zhang
  • Xiaoke Xu
  • Haigang Li
Original Article


Escherichia coli O157 is an important food-borne pathogen that can cause diarrhoea, haemorrhagic colitis, and haemolytic uraemic syndrome. The aim of this study was to investigate the prevalence, virulence genes, antibiotic resistance, and genetic diversity of E. coli O157 and O157:H7 in retail fresh raw meat sold in the markets of South China. Of 551 samples collected, 21 (3.81 %) were contaminated with E. coli O157 and seven (1.27 %) with O157:H7. The highest prevalence rate was found in beef (13.32 %), followed by pork (6.90 %), chicken (3.28 %), duck (2.54 %), and mutton (0). The virulence genes stx1, stx2, eaeA, and hlyA were detected in 10.71, 21.43, 85.71, and 25 % of 28 isolates, respectively. The isolates were highly resistant to penicillin (100 %), chloramphenicol (64.29 %), ampicillin (57.14 %), and sensitive to gentamicin (100 %), cefotazidime (96.43 %), and ciprofloxacin (96.43 %). Enterobacterial repetitive intergenic consensus-PCR (ERIC-PCR) classified 28 isolates and two reference strains into 19 different profiles with a discrimination index (D) of 0.961. Four E. coli O157:H7 isolates from beef showed 83 % similarity with the two clinical reference strains, indicating a potential high virulence for consumers. The results of this study suggested that fresh raw meat could be potential vehicles for transmission of E. coli O157 to humans.


Prevalence Virulence genes Antimicrobial resistance Enterobacterial repetitive intergenic consensus-PCR Escherichia coli O157 O157:H7 



This work was supported by research grants from the International Science and Technology Cooperation Projects (No.2013DFH30070). The authors acknowledge colleagues in our lab for kindly technical assistance. We are also thankful to the reviewers for their valuable suggestions and comments.

Supplementary material

13213_2015_1037_Fig2_ESM.gif (79 kb)
Supplemental files Figure S1

These are the results of multiple-PCR for identification of E .coli O157 and E. coli O157:H7 isolates. 1(a) Lanes: M, DNA size marker (DL2000); CK, negative control; 1, positive control ATCC35150; Lanes 2–8 are E. coli O157:H7 isolates (172–3, 202–2, 072–2, 075–1, 049–2, 050–2, 703–1). 1(b) Lanes: M, DNA size marker (DL2000); CK, negative control; 1, positive control ATCC35150; Lanes 2–22 are E. coli O157 isolates (1501–4, 142–2, 056–2, 230–3, 242–2, 2253–3, 2372–1, 2453–1, 073–3, 078–2, 236–1, 1552–1,054-1, 055–2, 009–1, 028–2, 175–4, 241–2, 225–2, 240–3, 016–3) (GIF 78 kb)

13213_2015_1037_MOESM1_ESM.tif (589 kb)
High Resolution Image (TIFF 588 kb)
13213_2015_1037_Fig3_ESM.gif (228 kb)
Supplemental files Figure S2

The geographic locations of the sampling sites in China. (GIF 228 kb)

13213_2015_1037_MOESM2_ESM.tif (357 kb)
High Resolution Image (TIFF 357 kb)


  1. Abong’o BO, Momba MN (2009) Prevalence and characterization of Escherichia coli O157:H7 isolates from meat and meat products sold in Amathole District, Eastern Cape Province of South Africa. Food Microbiol 26:173–176CrossRefPubMedGoogle Scholar
  2. Abu-Ali GS, Ouellette LM, Henderson ST, Whittam TS, Manning SD (2009) Differences in adherence and virulence gene expression between two outbreak strains of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 156:408–419CrossRefPubMedGoogle Scholar
  3. Ateba CN, Mbewe M (2011) Detection of Escherichia coli O157:H7 virulence genes in isolates from beef, pork, water, human and animal species in the northwest province, South Africa: public health implications. Res Microbiol 162:240–248CrossRefPubMedGoogle Scholar
  4. Bai L, Liu XM, Fu P, Guo YC (2010) Serotyping and virulence genes of suspected Escherichia coli O157 strains in food from 2005 to 2007. Wei Sheng Yan Jiu 39:335–339 (In Chinese)PubMedGoogle Scholar
  5. Bauer ME, Welch RA (1996) Characterization of an RTX toxin from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 64:167–175PubMedCentralPubMedGoogle Scholar
  6. Bell BP, Goldoft M, Griffin PM, Davis MA, Gordon DC, Tarr PI, Bartleson CA, Lewis JH, Barrett TJ, Wells JG (1994) A multistate outbreak of Escherichia coli O157:H7-associated bloody diarrhea and hemolytic uremic syndrome from hamburgers. The Washington experience. J Am Med Assoc 272:1349–1353CrossRefGoogle Scholar
  7. Bettelheim KA, Beutin L (2003) Rapid laboratory identification and characterization of verocytotoxigenic (shigatoxin-producing) Escerichia coli (VTEC/STEC). J Appl Microbiol 95:205–217CrossRefPubMedGoogle Scholar
  8. Beutin L, Krause G, Zimmermann S, Kaulfuss S, Gleier K (2004) Characterization of shiga toxin-producing Escherichia coli strains isolated from human patients in Germany over a 3-year period. J Clin Microbiol 42:1099–1108PubMedCentralCrossRefPubMedGoogle Scholar
  9. Blanco JE, Blanco M, Alonso MP, Mora A, Dahbi G, Coira MA, Blanco J (2004) Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from human patients: prevalence in Lugo, Spain, from 1992 through 1999. J Clin Microbiol 42:311–319PubMedCentralCrossRefPubMedGoogle Scholar
  10. Cadirci O, Siriken B, Inat G, Kevenk TO (2010) The prevalence of Escherichia coli O157 and O157:H7 in ground beef and raw meatball by immunomagnetic separation and the detection of virulence genes using multiplex PCR. Meat Sci 84:553–556CrossRefPubMedGoogle Scholar
  11. Cagney C, Crowley H, Duffy G, Sheridan JJ, O’Brien S, Carney E, Anderson W, Mcdowell DA, Blair IS, Bishop RH (2004) Prevalence and number of Escherichia coli O57: H7 in minced beef and beef burgers from butcher shops and supermarkets in the Republic of Ireland. Food Microbiol 21:203–212CrossRefGoogle Scholar
  12. Caro I, Fernández-Barata VM, Alonso-Llamazares A, García-Armesto MR (2006) Detection, occurrence, and characterization of Escherichia coli O157:H7 from raw ewe’s milk in Spain. J Food Prot 69:920–924PubMedGoogle Scholar
  13. Chen M, Wu QP, Zhang JM, Yan ZA, Wang J (2014) Prevalence and characterization of Listeria monocytogenes isolated from retail-level ready-to-eat foods in South China. Food Control 38:1–7CrossRefGoogle Scholar
  14. CLSI - Clinical and Laboratory Standards Institute (2006) Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria. Approved Standard M45-A. Clinical and Laboratory Standards Institute. Wayne, PAGoogle Scholar
  15. Dean-Nystrom EA, Bosworth BT, Cray WC Jr, Moon HW (1997) Pathogenicity of Escherichia coli O157:H7 in the intestines of neonatal calves. Infect Immun 65:1842–1848PubMedCentralPubMedGoogle Scholar
  16. Doane CA, Pangloli P, Richards HA, Mount JR, Golden DA, Draughon FA (2007) Occurrence of Escherichia coli O157:H7 in diverse farm environments. J Food Prot 70:6–10PubMedGoogle Scholar
  17. Goncuoglu M, Ormanci BFS, Ayaz ND (2010) Antibiotic resistance of Escherichia coli O157:H7 isolated from cattle and sheep. Ann Microbiol 60:489–494CrossRefGoogle Scholar
  18. Govaris A, Angelidis AS, Katsoulis K, Pournaras S (2011) Occurrence, virulence genes and antimicrobial resistance of Escherichia coli O157 in bovine, caprine, ovine and porcine carcasses in Greece. J Food Saf 31:242–249CrossRefGoogle Scholar
  19. Gyles CL (2007) Shiga toxin–producing Escherichia coli: an overview. J Anim Sci 85:45–62CrossRefGoogle Scholar
  20. Hiko A, Asrat D, Zewde G (2008) Occurrence of Escherichia coli O157:H7 in retail raw meat products in Ethiopia. J Infect Dev Ctries 11:1085–1092Google Scholar
  21. Hunter PR, Gaston MA (1988) Numerical index of the discriminatory ability of typing systems: an application of simpson’s index of diversity. J Clin Microbiol 26:2465–2466PubMedCentralPubMedGoogle Scholar
  22. Jo MY, Kim JH, Lim JH, Kang MY, Koh HB, Park YH, Yoon DY, Chae JS, Eo SK, Lee JH (2004) Prevalence and characteristics of Escherichia coli O157 from major food animals in Korea. Int J Food Microbiol 95:41–49CrossRefPubMedGoogle Scholar
  23. Lenahan M, O’Brien S, Kinsella K, Sweeney T, Sheridan JJ (2007) Prevalence and molecular characterization of Escherichia coli O157:H7 on Irish lamb carcasses, fleece and in faeces samples. J Appl Microbiol 103:2401–2409CrossRefPubMedGoogle Scholar
  24. Ling OW, Radu S, Rusul G, Karim MI, Purwati E, Lihan S (2000) Enterobacterial Repetitive Intragenic Consensus (ERIC) genotyping of Escherichia coli O157:H7. Pak J Biol Sci 3:35–37CrossRefGoogle Scholar
  25. Lukásová J, Abraham B, Cupáková S (2004) Occurrence of Escherichia coli O157 in raw material and food in Czech Republic. J Vet Med B 51:77–81CrossRefGoogle Scholar
  26. Magwira CA, Gashe BA, Collison EK (2005) Prevalence and antibiotic resistance profiles of Escherichia coli O157:H7 in beef products from retail outlets in Gaborone, Botswana. J Food Prot 68:403–406PubMedGoogle Scholar
  27. Olatoye IO (2010) The incidence and antibiotics susceptibility of Escherichia coli O157:H7 from beef in Ibadan Municipal, Nigeria. Afr J Biotechnol 9:1196–1199Google Scholar
  28. Paton AW, Paton JC (1998) Detection and characterization of shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfbO111, and rfbO157. J Clin Microbiol 36:598–602PubMedCentralPubMedGoogle Scholar
  29. Pradel N, Bertin Y, Martin C, Livrelli V (2008) Molecular analysis of shiga toxinproducing Escherichia coli strains isolated from haemolytic-uremic syndrome patients and dairy samples in France. Appl Environ Microbiol 74:2118–2128PubMedCentralCrossRefPubMedGoogle Scholar
  30. Rahimi E, Kazemeini HR, Salajegheh M (2012) Escherichia coli O157/NM prevalence in raw beef, camel, sheep, goat, and water buffalo meat in fars and Khuzestan provinces, Iran. Vet Res Forum 3:13–17Google Scholar
  31. Sallam KI, Mohammed MA, Ahdy AM, Tamura T (2013) Prevalence, genetic characterization and virulence genes of sorbitol-fermenting Escherichia coli O157:H- and E. coli O157:H7 isolated from retail beef. Int J Food Microbiol 165:295–301CrossRefPubMedGoogle Scholar
  32. Sarimehmetoglu B, Aksoy MH, Ayaz ND, Ayaz Y, Kuplulu O, Kaplan YZ (2009) Detection of Escherichia coli O157:H7 in ground beef using immunomagnetic separation and multiplex PCR. Food Control 20:357–361CrossRefGoogle Scholar
  33. Seker E, Kuyucuoğlu Y, Sareyyüpoğlu B, Yardımcı H (2010) PCR detection of Shiga toxins, enterohaemolysin and intimin virulence genes of Escherichia coli O157:H7 strains isolated from faeces of Anatolian water buffaloes in Turkey. Zoonoses Public Health 57:33–37CrossRefGoogle Scholar
  34. Stampi S, Caprioli A, De Luca G, Quaglio, Sacchetti R, Zanetti F (2004) Detection of Escherichia coli O157 in bovine meat products in northern Italy. Int J Food Microbiol 90:257–262CrossRefPubMedGoogle Scholar
  35. Swaminathan B, Barrett TJ, Hunter SB, Tauxe RV, PulseNet Task Force CDC (2001) PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis 7:382–389PubMedCentralCrossRefPubMedGoogle Scholar
  36. United States Department of Agriculture, Food Safety Inspection Service (2002) Detection, isolation and identification of Escherichia coli O157:H7 and O157:NM (Nonmotile) from meatGoogle Scholar
  37. Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831PubMedCentralCrossRefPubMedGoogle Scholar
  38. Villani F, Russo F, Blaiotta G, Moschetti G, Ercolini D (2005) Presence and characterisation of verotoxin producing E. coli in fresh Italian pork sausages, and preparation and use of an antibiotic-resistant strain for challenge studies. Meat Sci 70:181–188CrossRefPubMedGoogle Scholar
  39. Xu XK, Wu QP, Zhou YH, Zhang JM, Yang XJ (2008) Specific and sensitive detection of Escherichia coli O157:H7 in meat by a multiplex PCR. Microbiol China 35:619–622 (In Chinese)Google Scholar
  40. Ye YW, Wu QP, Yao L, Dong XH, Wu K, Zhang JM (2009) Analysis of a consensus fragment in ERIC-PCR fingerprinting of Enterobacter sakazakii. Int J Food Microbiol 132:172–175CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg and the University of Milan 2015

Authors and Affiliations

  • Shuhong Zhang
    • 1
  • Xuemei Zhu
    • 1
  • Qingping Wu
    • 1
    Email author
  • Jumei Zhang
    • 1
  • Xiaoke Xu
    • 1
  • Haigang Li
    • 1
  1. 1.State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Public Laboratory for Applied and New Technology of Microbiology, Guangdong Provincial Key Laboratory of Microbial Culture Collection and ApplicationGuangdong Institute of MicrobiologyGuangzhouChina

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