Enterotoxigenicity and Antimicrobial Resistance of Staphylococcus aureus Isolated from Retail Food in China

Wang, Wei; Baloch, Zulqarnain; Jiang, Tao; Zhang, Cunshan; Peng, Zong–Gen; Li, Fengqin; Fanning, Séamus; Ma, Aiguo; Xu, Jin

doi:10.3389/fmicb.2017.02256

Cited by 76 publications

(84 citation statements)

References 58 publications

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“…Most of the MRSA strains were resist to β-lactams and other antibiotics which showed 77.4% (48/62) were resistant to more than 10 antibiotics. This result as similar with the results of research by Wang et al ( 2017 ) and Hao et al ( 2015 ) in China. In fact, the prevalence of MRSA varies greatly by geographical location in retail meats.…”

Section: Discussionsupporting

confidence: 93%

“…In China, (Xing et al, 2014 ) revealed that 98.4% of S. aureus isolates in ready-to-eat food were resist to more than one antimicrobial agent and 58.6% of isolates resist to more than three antimicrobials, while (Hao et al, 2015 ) found that 35.9% of S. aureus isolated from quick-frozen dumpling were resistant to less than or equal to 3 kinds of drugs. In Wang et al ( 2017 ) reported that 97.6% of S. aureus isolates from retail food showed resistance in one or more antimicrobial agents. The prevalence of resistance to clindamycin, gentamicin, penicillin, erythromycin, tetracycline, and ciprofloxacin is in agreement with our data.…”

Section: Discussionmentioning

confidence: 99%

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Staphylococcus aureus Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity

Wu¹,

Huang²,

Wu³

et al. 2018

Front. Microbiol.

148

107

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This study was to estimate the prevalence and characteristics of Staphylococcus aureus from 1,850 retail meat and meat products in China during July 2011 to June 2016. The samples were collected covering most provincial capitals in China, including 604 raw meat, 601 quick-frozen meat, and 645 ready-to-eat meat. Using the qualitative and quantitative methods, all 39 cities had S. aureus-positive samples, and S. aureus was detected in 35.0% (647/1,850) of the samples. The levels of S. aureus in retail meat showed that the MPN value of the majority of the positive samples ranged from 0.3 to 100 MPN/g. Twenty-four antibiotics were used to test all 868 S. aureus isolates for antibiotic susceptibility. Only 11 isolates (1.26%) were susceptible to all antibiotics, whereas most isolates (821/868, 94.6%) showed resistance or intermediary resistance to more than three or more antibiotics. Of these strains, 104 (12.0%) were resistant to more than 10 antibiotics. However, the most frequent resistance was observed to ampicillin (85.4%), followed by penicillin (84.6%), erythromycin (52.7%), tetracycline (49.3%), kanamycin (45.3%), telithromycin (30.1%), clindamycin (29.6%), streptomycin (21.1%), norfloxacin (20.4%), gentamicin (19.4%), fusidic acid (18.4%), ciprofloxacin (16.9%), chloramphenicol (13.1%), amoxycillin/clavulanic acid (11.0%), and others (<10%). 7.4% of isolates (62/868) were confirmed as methicillin-resistance S. aureus (MRSA). By molecular typing analysis, there were 164 spa types and 111 STs were identified, including 15 novel spa types and 65 newly STs by multilocus sequence typing (MLST) and spa typing. Despite the wide genetic diversity observed among the 868 isolates, a great proportion of the population belonged to finite number of major clones: ST1-t127 (93/868, 10.7%) and ST7-t091 (92/868, 10.6%), ST5-t002 (42/868, 4.8%), ST398-t034 (40/868, 4.6%), ST188-t034 (38/868, 4.4%), ST59-t437 (30/868, 3.5%), ST6-t701 (29/868, 3.3%), and ST9-t899 (27/868, 3.1%) in China. This study reflects S. aureus was readily detected in Chinese retail meat and meat products but the level were not very excessive. In this study, the high antibiotic resistance is alarming and raising public health concern. In additions, most of molecular types of isolates have been linked to human infections around the world, indicating that these types of S. aureus in China have a theoretical pathogenic potential.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Staphylococcus aureus Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity

Wu¹,

Huang²,

Wu³

et al. 2018

Front. Microbiol.

148

107

View full text Add to dashboard Cite

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“…As reported by many authors, raw milk has been identified as a source of MRSA demonstrating the potential food safety of contaminated milk and dairy products entering the human food chain (Carfora et al 2015;Caruso et al 2016;Parisi et al 2016;Basanisi et al 2017;Giaciniti et al 2017;Papadopoulos et al 2019b;Titouche et al 2019). However, MRSA was also isolated in meat (De Boer et al 2009;Hanson et al 2011;Thapaliya et al 2017;Tang et al 2017) and from ready to eat products (Wang et al 2017;Islam et al 2019). To date, a great number of studies reported the isolation of MRSA from livestock, wild animals and derived foods, both raw and ready to eat, as well as from professionals working in animal husbandry or the food production chain settings (Sergelidis and Angelidis 2017).…”

Section: Discussionmentioning

confidence: 86%

Enterotoxin genes and antimicrobial resistance in Staphylococcus aureus isolated from food products in Algeria

Titouche

Houali

Ruiz-Ripa

et al. 2020

J. Appl. Microbiol.

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Aims The aim of this study was to characterize Staphylococcusaureus isolates of food origin (dairy and meat products, pastries and sandwiches) determining the carriage in enterotoxin genes and the antimicrobial resistance pheno/genotypes. Methods and results A total of 300 food samples were collected and analysed for the detection of S. aureus. The presence of enterotoxin genes was investigated by multiplex PCRs. Resistance of isolates to 11 antimicrobials was determined using disc diffusion method and molecular characterization of methicillin‐resistant S. aureus was carried out by spa typing and multilocus sequence typing. Overall, 51 out of 300 samples (17%) were contaminated with S. aureus, and 104 isolates were recovered. In all, 65 of these isolates (62·5%) harboured one or more genes encoding for staphylococcal enterotoxins, being seg and sei the most observed genes. The highest resistance profile was ascribed to penicillin G (95·19%). Five isolates were methicillin‐resistant (MRSA) harbouring the mecA gene. All MRSA isolates belonged to the sequence type ST5 and to two different spa types (t450 and t688); the MRSA‐t450 isolate carried the scn gene (specific marker of the immune evasion cluster system), but the four MRSA‐t688 isolates were scn negative. The MRSA isolates carried enterotoxin genes but were negative for the genes of the Panton Valentine leukocidine (lukF/S‐PV). Conclusion The presence of enterotoxigenic S. aureus isolates, including MRSA, in food samples can represent a risk for public health. Significance and Impact of this Study This work describes the molecular characteristics of MRSA strains isolated from foods in Algeria and it can contribute to an extended database concerning the S. aureus isolated from food origin.

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“…In recent years, the spread of antibiotic resistance among strains of S. aureus is of great public and clinical concern in the treatment of staphylococcal infections (Shankar, 2012 ). Many researchers have reported resistance strains of S. aureus isolates from various food samples in different countries (Argudín et al, 2012 ; Yang et al, 2016b ; Wang et al, 2017 ). In the current study, 76.7% of vegetable S. aureus isolates (23/30) were resistant or intermediate resistant to more than three tested antibiotics classes, of which 9 isolates were resistant to more than 10 antibiotics.…”

Section: Discussionmentioning

confidence: 99%

Prevalence and Characterization of Staphylococcus aureus Isolated From Retail Vegetables in China

Huang

et al. 2018

Front. Microbiol.

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Staphylococcus aureus is a pathogen associated with serious community and hospital-acquired diseases. The aim of this study was to investigate the prevalence of S. aureus from retail vegetables in China and then characterized S. aureus isolates by antibiotic resistance, staphylococcal enterotoxin genes, spa-typing and multi-locus sequence typing. Of 419 retail vegetable samples from 39 cities in China during 2011–2016, 24 (5.73%) samples were positive for S. aureus and the geometric mean was 3.85 MPN/g. The prevalence of S. aureus was highest in lettuce (13/84, 15.48%) followed by tomato (7/110, 6.36%), caraway (2/87, 2.30%), and cucumber (2/128, 1.56%), whereas other vegetables were free of S. aureus. A total of 30 isolates were analyzed. For antibiotics susceptibility test, most isolates (93.3%) were resistant to ampicillin and penicillin, whereas all isolates were susceptible to linezolid, trimethoprim/sulphamethoxazole 1:19, nitrofurantoin, rifampicin, and teicoplanin. All isolates (30/30, 100%) were resistant or intermediate resistant to more than three tested antibiotics, including 9 isolates (30%) were resisted more than 10 antibiotics. Five isolates were resistant to cefoxitin and carried mecA genes which confirmed as MRSA. Of the 18 investigated SE genes, the sem gene was the most frequently detected (86.7%) followed by the sec (83.3%), sep (70.0%), seg (56.7%), sel (53.3%), seh (50.0%), seq (50.0%), sej (46.7%), seb (36.7%), sen (36.7%), and ser (33.3%) genes were harbored by more than one third of the isolates, whereas the seo and seu were detected in only 6.75% of the isolates. MLST and spa typing observed high genetic diversity in S. aureus isolated from retail vegetable in China. ST59-t437 was the predominant types (3/5, 60%) of MRSA isolates, whereas ST188-t189 was the predominant types (7/25, 28%) of MSSA isolates. Our study reflects that the retail vegetable in China could be contaminated with S. aureus but the levels of S. aureus were not very excessive. In addition, these isolates had virulence potential, most of them were enterotoxigenic and multiple antimicrobial resistance, should be draw public attention. These data have signification implications for epidemiological and public health studies of this pathogen.

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Enterotoxigenicity and Antimicrobial Resistance of Staphylococcus aureus Isolated from Retail Food in China

Cited by 76 publications

References 58 publications

Staphylococcus aureus Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity

Staphylococcus aureus Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity

Enterotoxin genes and antimicrobial resistance in Staphylococcus aureus isolated from food products in Algeria

Prevalence and Characterization of Staphylococcus aureus Isolated From Retail Vegetables in China

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