Characterization of antimicrobial-resistant Staphylococcus aureus from retail foods in Beijing, China

doi:10.1016/j.fm.2020.103603

Food Microbiology

Volume 93, February 2021, 103603

https://doi.org/10.1016/j.fm.2020.103603 Get rights and content

Highlights

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The aerobic mesophilic counts were 5.5 ± 1.5 log CFU/g for sushi products and 5.6 ± 0.8 log CFU/g for pork products.
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Three MRSA strains were resistant to at least three classes of antimicrobials and thus designated as multidrug-resistant.
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Six lineages of S. aureus were detected: ST398 (n = 5), ST25 (n = 4), ST15 (n = 2), ST59 (n = 2), ST8 (n = 1) and ST2631 (n = 1).
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The MRSA isolates contained scn and enterotoxin genes.

Abstract

Staphylococcus aureus is an opportunistic pathogen leading to food poisoning as well as human infections. The present study examined the prevalence and characterization of antimicrobial-resistant S. aureus in sushi from 42 outlets and in pork products from eight outlets in Beijing, China. The total bacterial counts were between 3.0 and 8.9 log CFU/g (mean 5.5 ± 1.5 log CFU/g) in sushi products and 4.8 to 7.4 log CFU/g (mean 5.6 ± 0.8 log CFU/g) in pork products. The mean counts of coliforms were 2.7 and 2.9 log CFU/g in sushi and pork, respectively. Staphylococcus aureus was isolated from seven sushi outlets (13 isolates) and two pork outlets (2 isolates) with average counts below 2 log CFU/g in all cases. A total of 15 S. aureus isolates were further characterized. Six lineages of S. aureus were present, including ST398 (n = 5), ST25 (n = 4), ST15 (n = 2), ST59 (n = 2), ST8 (n = 1) and ST2631 (n = 1). Thirteen isolates contained the scn virulence marker, whereas four and eight isolates contained the virulence marker edinB and enterotoxin genes, respectively. Characterization of antimicrobial resistance profiles documented resistances to ampicillin (n = 15), penicillin (n = 14), ceftazidime (n = 6), erythromycin (n = 4), tetracycline (n = 3), clindamycin (n = 3), and gentamicin (n = 1). Three MRSA isolates were obtained, one from pork (ST398) and two from one sushi outlet (ST59). They were all resistant to at least three classes of antimicrobials and two of them contained the scn gene and enterotoxin genes. Twelve sushi isolates and one of the pork isolates contained the scn gene, indicating that they were of human origin. This emphasizes the potential importance of transmission through foods of antimicrobial-resistant S. aureus including MRSA. We also showed that S. aureus exhibited geographical variation with regards to ST profiles, antimicrobial-resistance and virulence genes when comparing isolates from sushi products sold in Beijing and Copenhagen, Denmark. Whereas food safety is not compromised by the presence of low amounts of S. aureus in sushi, this study shows that with regards to public health such foods may serve as vehicles for transmission of multidrug-resistant S. aureus and MRSA lineages.

Introduction

Ready-to-eat (RTE) food products might serve as potential vehicles for transmission of antimicrobial-resistant bacteria due to manual handling or contaminated raw materials (Marshall and Levy, 2011; Li et al., 2019b). Staphylococcus aureus is an opportunistic pathogen that may cause food poisoning as well as human clinical infections. There is increasing concern regarding the presence of foodborne S. aureus encoding antimicrobial resistance and/or virulence phenotypes and in particular methicillin-resistant (MRSA) variants (Vandenesch et al., 2003; Kluytmans, 2010; Tang et al., 2017; Luo et al., 2018; Wu et al., 2019). MRSA exhibit resistance to β-lactam antibiotics by acquisition of the mobile staphylococcal cassette chromosome mec (SCCmec) (Chaję̨cka-Wierzchowska et al., 2014; Kadariya et al., 2014). In China, regional surveillance of S. aureus in RTE foods from twenty-four cities between 2011 and 2014 reported that 12.5% were positive for S. aureus including MRSA strains identified as ST9, ST59, ST339, and ST3239 (Yang et al., 2016). In a study from the central area of China, the main spa types of human clinical isolates were t002, t030, t189 and t437, while it was the case of t002, t091, t127 and t189, in food products (Luo et al., 2018).

In our previous work, we investigated the antimicrobial resistance and virulence profiles of methicillin-sensitive S. aureus (MSSA) and MRSA variants from ready-to-eat Danish sushi and pasta salad products as well as retail meat (Tang et al., 2017; Li et al., 2019b). The prevalence of genotypes and clonal distribution among S. aureus human clinical isolates may depend on geographical locations (Asadollahi et al., 2018), e.g. MSSA ST7, ST188 and ST398 represented the top three types of S. aureus bacteremia infections in China while it was the ST1, ST5, and ST15 MSSA types in Danish bacteremia cases. In a MRSA context, ST59 and ST239 were the predominant clones in Chinese bacteremia cases while MRSA ST5, ST8 and ST22 were commonly implicated in Danish bacteremia cases (DANMAP, 2018; Li et al., 2018). On the contrary, MRSA from the ST398 lineage appears to be able to colonize pigs on a global scale (Smith and Pearson, 2011; Price et al., 2012). The present study aimed to illuminate whether food-borne isolates of S. aureus exhibit geographical variation by examination of prevalence, genotypes, antimicrobial-resistance and virulence gene profiles of S. aureus isolated from sushi or pork meat sold in Beijing, China and by comparing their profiles to those previously found in Danish food isolates.

Section snippets

Materials and methods

A total of 50 outlets including 42 sushi shops and eight supermarkets were examined between October and November 2019 in Beijing. The outlets were located in the western and northwestern suburban districts of Beijing city, including Changping (n = 2), Haidian (n = 33) and Shijingshan (n = 15) (Fig. 1; Table S1). Packages of Maki sushi and sliced raw pork were purchased and transported to the laboratory on ice bags for analysis that was initiated within 4 h of collection. The mean weight of the

Results and discussion

The total aerobic bacterial counts of sushi products were between 3.0 and 8.9 log CFU/g with a mean of 5.5 ± 1.5 log CFU/g and between 4.8 and 7.4 log CFU/g for pork products with a mean of 5.6 ± 0.8 log CFU/g (Table 1). The mean counts of coliforms were 2.7 and 2.9 log CFU/g while mean counts of Staphylococcus spp. were 3.3 and 3.9 log CFU/g in sushi and pork, respectively (Table 1 for details). Notably, S. aureus was only isolated from a minority of the Chinese products (n = 7 (16.6%) from

Conclusion

Our study analyzed the bacterial content and characterized antimicrobial-resistant S. aureus from sushi (16.7%; n = 7) and pork (25.0%; n = 2) in Beijing, China. Six lineages of S. aureus were found, including ST8, ST15, ST25, ST59, ST398, and ST2631. ST25 and ST59 are also the types often detected among human isolates from China. This study shows evidence for geographical variation of S. aureus isolates from sushi sold in Beijing and Copenhagen. Contrarily, ST398 that was detected in pork

Ethical approval

Not required.

Permission

Bacteria isolates were obtained with the approval from China Agricultural University.

Funding

This work was supported by a PhD study grant (CSC No. 201606350038) to Heng Li from China Scholarship Council. The authors also acknowledge funding support to Tianlong Liu from Beijing Natural Science Foundation (Grant no. 6202017) and Young Teachers Innovation Project of China Agricultural University (Grant no. 2018QC142).

Declaration of competing interest

The authors declare that there is no conflict of interest regarding the publication of this paper.

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¹: These two authors contributed equally to this work.

View full text

Characterization of antimicrobial-resistant Staphylococcus aureus from retail foods in Beijing, China

Highlights

Abstract

Introduction

Section snippets

Materials and methods

Results and discussion

Conclusion

Ethical approval

Permission

Funding

Declaration of competing interest

J. Food Protect.

Int. J. Food Microbiol.

Clin. Microbiol. Infect.

Int. J. Food Microbiol.

Front. Microbiol.

Int. J. Food Microbiol.

Int. J. Food Microbiol.

FEMS Microbiol. Lett.

Distribution of the most prevalent spa types among clinical isolates of methicillin-resistant and-susceptible Staphylococcus aureus around the world: a review

Front. Microbiol.

Plasmid and clonal interference during post horizontal gene transfer evolution

Mol. Ecol.

Staphylococcal enterotoxins and enterotoxin-like toxins with special reference to dairy products: an overview

Crit. Rev. Food Sci. Nutr.

EDIN-B promotes the translocation of Staphylococcus aureus to the bloodstream in the course of pneumonia

Toxins

Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Food and Humans in Denmark

Whole genome sequencing of Danish Staphylococcus argenteus reveals a genetically diverse collection with clear separation from Staphylococcus aureus

Front. Microbiol.

Typing of vancomycin-resistant enterococci with MALDI-TOF mass spectrometry in a nosocomial outbreak setting

Clin. Microbiol. Infect.

Solving the problem of comparing whole bacterial genomes across different sequencing platforms

PloS One