High prevalence and pathogenic potential of Shiga toxin-producing Escherichia coli strains in raw mutton and beef in Shandong, China

doi:10.1016/j.crfs.2022.08.021

. 2022 Sep 15:5:1596-1602.

doi: 10.1016/j.crfs.2022.08.021. eCollection 2022.

High prevalence and pathogenic potential of Shiga toxin-producing Escherichia coli strains in raw mutton and beef in Shandong, China

Bin Hu¹, Xi Yang², Qian Liu², Yuanqing Zhang¹, Deshui Jiang³, Hongbo Jiao³, Ying Yang¹, Yanwen Xiong², Xiangning Bai^{2

4}, Peibin Hou¹

Affiliations

¹ Shandong Center for Disease Control and Prevention, Jinan, 250014, Shandong, China.
² State Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, 102206, China.
³ Lanling Center for Disease Control and Prevention, Lanling, 277700, Shandong, China.
⁴ Division of Clinical Microbiology, Department of Laboratory Medicine, Karolinska Institute, 141 52, Stockholm, Sweden.

PMID: 36161222
PMCID: PMC9493282
DOI: 10.1016/j.crfs.2022.08.021

High prevalence and pathogenic potential of Shiga toxin-producing Escherichia coli strains in raw mutton and beef in Shandong, China

Bin Hu et al. Curr Res Food Sci. 2022.

. 2022 Sep 15:5:1596-1602.

doi: 10.1016/j.crfs.2022.08.021. eCollection 2022.

Authors

Bin Hu¹, Xi Yang², Qian Liu², Yuanqing Zhang¹, Deshui Jiang³, Hongbo Jiao³, Ying Yang¹, Yanwen Xiong², Xiangning Bai^{2

4}, Peibin Hou¹

Affiliations

¹ Shandong Center for Disease Control and Prevention, Jinan, 250014, Shandong, China.
² State Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, 102206, China.
³ Lanling Center for Disease Control and Prevention, Lanling, 277700, Shandong, China.
⁴ Division of Clinical Microbiology, Department of Laboratory Medicine, Karolinska Institute, 141 52, Stockholm, Sweden.

PMID: 36161222
PMCID: PMC9493282
DOI: 10.1016/j.crfs.2022.08.021

Abstract

Shiga toxin-producing Escherichia coli (STEC) is a foodborne pathogen that can cause severe human diseases such as hemolytic uremic syndrome (HUS). Human STEC infections are frequently caused through consumption of contaminated foods, especially raw meats. This study aimed to investigate the prevalence of STEC in raw meats and to characterize the meat-derived STEC strains using whole genome sequencing. Our study showed that 26.6% of raw mutton, and 7.5% of raw beef samples were culture-positive for STEC. Thirteen serotypes were identified in 22 meat-derived isolates in this study, including the virulent serotypes O157:H7 and O26:H11. Seven Shiga toxin (Stx) subtypes were found in 22 isolates, of these, stx1c and stx1c + stx2b were predominant. The recently-reported stx2k subtype was found in three mutton-sourced isolates. A number of other virulence genes such as genes encoding intimin (eae), enterohemorrhagic E. coli (EHEC) hemolysin (ehxA), EHEC factor for adherence (efa1), heat-stable enterotoxin 1 (astA), type III secretion system effectors, were detected in meat-derived STEC strains. One mutton-sourced isolate was resistant to three antibiotics, i.e., tetracycline, chloramphenicol, and trimethoprim-sulfamethoxazole. Whole-genome phylogeny indicated the genomic diversity of meat-derived strains in this study. O157:H7 and O26:H11 isolates in this study were phylogenetically grouped together with strains from HUS patients, suggesting their pathogenic potential. To conclude, our study reported high STEC contaminations in retail raw meats, particularly raw mutton, genomic characterization indicated pathogenic potential of meat-derived STEC strains. These findings highlight the critical need for increased monitoring of STEC in retail raw meats in China.

Keywords: Beef; Contamination; Mutton; Raw meats; Shiga toxin-producing Escherichia coli; Whole genome sequencing.

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Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

**Fig. 1**
**Whole-genome phylogeny of Shiga toxin-producing *Escherichia coli* (STEC) isolates.** Strain, serotype, *stx* subtype, MLST, and accession number of all STEC isolates are shown. The source of isolates, i.e., mutton, beef, and human clinical reference O157:H7 and O26:H11 isolates, are marked as indicated. Isolates from raw meats in this study are highlighted in green shadow. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

**figs1**
Phylogenetic tree based on single-nucleotide polymorphisms (SNPs) using the Maximum-Likelihood method. Branch length is ignored for better visualization. The source and serotype of strains are shown. The heatmap illustrates pairwise SNP distances between the STEC isolates.

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[1] Bai X., Scheutz F., Dahlgren H.M., Hedenstrom I., Jernberg C. Characterization of clinical Escherichia coli strains producing a novel Shiga toxin 2 subtype in Sweden and Denmark. Microorganisms. 2021;9(11) doi: 10.3390/microorganisms9112374. - DOI - PMC - PubMed

[2] Bai X., Scheutz F., Dahlgren H.M., Hedenstrom I., Jernberg C. Characterization of clinical Escherichia coli strains producing a novel Shiga toxin 2 subtype in Sweden and Denmark. Microorganisms. 2021;9(11) doi: 10.3390/microorganisms9112374. - DOI - PMC - PubMed

[3] Bai X., Wang H., Xin Y., Wei R., Tang X., Zhao A.…Xiong Y. Prevalence and characteristics of Shiga toxin-producing Escherichia coli isolated from retail raw meats in China. Int. J. Food Microbiol. 2015;200:31–38. doi: 10.1016/j.ijfoodmicro.2015.01.018. - DOI - PubMed

[4] Bai X., Wang H., Xin Y., Wei R., Tang X., Zhao A.…Xiong Y. Prevalence and characteristics of Shiga toxin-producing Escherichia coli isolated from retail raw meats in China. Int. J. Food Microbiol. 2015;200:31–38. doi: 10.1016/j.ijfoodmicro.2015.01.018. - DOI - PubMed

[5] Bai X., Zhang J., Hua Y., Jernberg C., Xiong Y., French N.…Matussek A. Genomic insights into clinical Shiga toxin-producing Escherichia coli strains: a 15-year period survey in Jönköping, Sweden. Front. Microbiol. 2021;12 doi: 10.3389/fmicb.2021.627861. - DOI - PMC - PubMed

[6] Bai X., Zhang J., Hua Y., Jernberg C., Xiong Y., French N.…Matussek A. Genomic insights into clinical Shiga toxin-producing Escherichia coli strains: a 15-year period survey in Jönköping, Sweden. Front. Microbiol. 2021;12 doi: 10.3389/fmicb.2021.627861. - DOI - PMC - PubMed

[7] Bielaszewska M., Aldick T., Bauwens A., Karch H. Hemolysin of enterohemorrhagic Escherichia coli: structure, transport, biological activity and putative role in virulence. Int J Med Microbiol. 2014;304(5–6):521–529. doi: 10.1016/j.ijmm.2014.05.005. - DOI - PubMed

[8] Bielaszewska M., Aldick T., Bauwens A., Karch H. Hemolysin of enterohemorrhagic Escherichia coli: structure, transport, biological activity and putative role in virulence. Int J Med Microbiol. 2014;304(5–6):521–529. doi: 10.1016/j.ijmm.2014.05.005. - DOI - PubMed

[9] Brashears M.M., Chaves B.D. The diversity of beef safety: a global reason to strengthen our current systems. Meat Sci. 2017;132:59–71. doi: 10.1016/j.meatsci.2017.03.015. - DOI - PubMed

[10] Brashears M.M., Chaves B.D. The diversity of beef safety: a global reason to strengthen our current systems. Meat Sci. 2017;132:59–71. doi: 10.1016/j.meatsci.2017.03.015. - DOI - PubMed

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High prevalence and pathogenic potential of Shiga toxin-producing Escherichia coli strains in raw mutton and beef in Shandong, China

Affiliations

High prevalence and pathogenic potential of Shiga toxin-producing Escherichia coli strains in raw mutton and beef in Shandong, China

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

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