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.
Staphylococcus aureus, particularly methicillin-resistant S.aureus (MRSA), is a life-threatening pathogen in humans, and its presence in food is a public health concern. MRSA has been identified in foods in China, but little information is available regarding MRSA in ready-to-eat (RTE) foods. We aimed to investigate the prevalence of S. aureus and MRSA in Chinese retail RTE foods. All isolated S. aureus were tested for antimicrobial susceptibility, and MRSA isolates were further characterized by multilocus sequence typing (MLST) and staphylococcal cassette chromosome mec (SCCmec) typing. Of the 550 RTE foods collected from 2011 to 2014, 69 (12.5%) were positive for S. aureus. Contamination levels were mostly in the range of 0.3–10 most probable number (MPN)/g, with five samples exceeding 10 MPN/g. Of the 69 S. aureus isolates, seven were identified as MRSA by cefoxitin disc diffusion test. Six isolates were mecA-positive, while no mecC-positive isolates were identified. In total, 75.8% (47/62) of the methicillin-susceptible S. aureus isolates and all of the MRSA isolates were resistant to three or more antibiotics. Amongst the MRSA isolates, four were identified as community-acquired strains (ST59-MRSA-IVa (n = 2), ST338-MRSA-V, ST1-MRSA-V), while one was a livestock-associated strain (ST9, harboring an unreported SCCmec type 2C2). One novel sequence type was identified (ST3239), the SCCmec gene of which could not be typed. Overall, our findings showed that Chinese retail RTE foods are likely vehicles for transmission of multidrug-resistant S. aureus and MRSA lineages. This is a serious public health risk and highlights the need to implement good hygiene practices.
Methicillin-resistant Staphylococcus aureus (MRSA) is an emerging pathogen that is difficult to treat due to the multiresistance of the bacteria upon infection. From 2011 to 2016, 1581 S. aureus strains were isolated from 4300 samples from retail foods covering most provincial capitals in China. To determine the prevalence of food-related MRSA and its genetic background in China, antibiotic resistance, staphylococcal toxin genes, staphylococcal cassette chromosome mec ( SCCmec ) typing, spa -typing and MLST were carried out in this study. In total, 108 (7.4%) isolates were confirmed for MRSA by phenotyping (cefoxitin) and genotyping ( mecA/mecC gene). A total of 52.8% (57/108) of the MRSA isolates belonged to clonal complex 59 (CC59) (ST59, ST338, and ST3355), which was the predominant clone in this study. These CC59 isolates carried SCC mec elements of type IV, V, or III and exhibited spa type t437, t441, t543, t163, t1785, or t3485, and half of them carried major virulence genes, such as the Panton-Valentine leucocidin (PVL) gene. The secondary clones belonged to ST9 (15.7%, 17/108) with a type of t899-SCC mec III and showed a broader range of antimicrobial resistance. The remaining MRSA isolates (31.5%, 34/108) were distributed in 12 different STs and 18 different spa types. All isolates harbored at least one of the enterotoxin genes, whereas only 4 isolates (3.70%) were positive for the toxic shock syndrome toxin tsst alleles. For antibiotic susceptibility testing, all isolates were resistant to more than three antibiotics, and 79.6% of the isolates were resistant to more than 10 antibiotics. Amoxycillin/clavulanic acid, ampicillin, cefoxitin, penicillin, ceftazidime, kanamycin, streptomycin, clindamycin, and telithromycin was the most common antibiotic resistance profile (55.6%, 60/108) in the study. In summary, the results of this study implied that the major food-related MRSA isolate in China was closer to community-associated MRSA, and some of the remaining isolates (ST9-t899-SCC mec III) were supposed to livestock-associated MRSA. In addition, most MRSA isolates showed resistance to multiple drugs and harbored staphylococcal toxin genes. Thus, the pathogenic potential of these isolates cannot be ignored. In addition, further studies are needed to elucidate the transmission routes of MRSA in relation to retail foods and to determine how to prevent the spread of MRSA.
Staphylococcus aureus is one of the most important food-borne pathogens globally. It produces various toxins and invasive enzymes and can be found in numerous food products. Milk is an important source of staphylococcal food poisoning. After pasteurization, this microorganism or its enterotoxins might still remain in pasteurized milk. Therefore, this study was to investigate the contamination of S. aureus in 258 pasteurized milk from 39 cities of China. The prevalence and levels of S. aureus in these samples as well as antibiotic susceptibility profiles, virulence genes, biofilm formation, and biofilm related genes, spa typing and MLST were used to determine the characterization among the isolates. It was found 3.9% of samples were detected S. aureus in 8 of 39 cities in China. The contaminated level were not very excessive which showed the MPN values of the most positive samples (9/10) were less than 1 MPN/g. All pasteurized milk-related S. aureus isolates have ability to produce biofilm and harbored icaA, icaD, eno , clfA, clfB, fnbA, fnbB, fib genes, other biofilm related genes icaC were showed in 91.7% of isolates and cna gene were showed in 50%, except bap gene which were free in all isolates. The antibiotic susceptibility test showed that all isolates were resistant or intermediate-resistant to different concentrations of the antibiotics. Furthermore, 75.0% of the isolates were resistant to three or more antibiotic classes, which indicated multidrug resistance. The isolates had virulence potential, which showed 66.7% (8/12) of the isolates carried one or more virulence-associated genes. Molecular typing by MLST and spa typing enabled classification of these isolates into a total of 11 sequence types (STs) and spa types, which indicated high genetic diversity. Most of these types were related to various clinical S. aureus infections. Thus, the findings of this study reflect the potential risk of S. aureus infection in China. Our study also provides comprehensive analysis of the prevalence of S. aureus in pasteurized milk and helps ensure more accurate treatment of human infection with effective antibiotics.
Salmonella remains the leading cause of reported bacterial foodborne disease in China. Meat products are recognized as one of the major sources of human salmonellosis; however, there is a lack of comprehensive, quantitative data concerning Salmonella contamination of these foods. Therefore, the objectives of this study were to investigate the prevalence, bacterial load, and antimicrobial resistance profiles of various Salmonella serovars in retail meat across the whole of China. Between July 2011 and June 2016, a total of 807 retail meat samples were collected, covering most provincial capitals in China. Overall, 159 (19.7%) samples tested positive for Salmonella. The highest contamination rate occurred in pork (37.3%, n = 287), followed by beef (16.1%, n = 161), mutton (10.9%, n = 92), dumplings (6.6%, n = 212), and smoked pork (3.6%, n = 55). Most probable number (MPN) analysis revealed that contamination was mainly in the range of 0.3–10 MPN/g among those samples testing positive using this method (n = 83), with eight samples exceeding 110 MPN/g. Among the 456 Salmonella enterica subsp. enterica isolates obtained in this study, 29 serovars and 33 multilocus sequence typing patterns were identified, with S. Derby, S. Typhimurium, S. London, S. Rissen, S. 1,4,[5],12:i:-, S. Weltevreden, and S. Enteritidis being the most prevalent. Among the 218 non-duplicate isolates, 181 (83.0%) were resistant to at least one class of antimicrobials and 128 (58.7%) were resistant to at least three classes. High rates of resistance were observed for tetracycline (65.6%), ampicillin (45.4%), trimethoprim-sulfamethoxazole (40.8%), streptomycin (40.4%), and nalidixic acid (35.8%), with the seven most prevalent serovars, except S. Weltevreden, showing higher rates of resistance and multidrug resistance compared with the less dominant serovars. Of note, all S. Indiana isolates exhibited resistance to extended-spectrum cephalosporins (including ceftriaxone and cefepime), ciprofloxacin, and multiple other classes of antibiotics. Further, two S. 1,4,[5],12:i:- isolates showed resistance to imipenem. This study provides systematic and comprehensive data on the prevalence and antimicrobial resistance profiles of various Salmonella serovars isolated from meat products in China, indicating their potential risk to public health.
Salmonella enterica subsp. enterica serovar 1,4,[5],12:i:- is a monophasic variant of Salmonella Typhimurium, which has recently been recognized as an emerging cause of infection worldwide. This bacterium has also ranked among the four most frequent serovars causing human salmonellosis in China. However, there are no reports on its contamination in Chinese food. Serotyping, polymerase chain reaction, antibiotic resistance, virulotyping, and multilocus sequence typing (MLST) assays were used to investigate the prevalence of this serological variant in food products in China, and to determine phenotypic and genotypic difference of monophasic isolates and Salmonella Typhimurium isolated over the same period. Salmonella 1,4,[5],12:i:- was prevalent in various food sources, including beef, pork, chicken, and pigeon. The study also confirmed the high prevalence (53.8%) of resistance to ampicillin, streptomycin, sulfonamides, and tetracycline in Salmonella 1,4,[5],12:i:-, which was higher than that in Salmonella Typhimurium. Moreover, Salmonella 1,4,[5],12:i:- isolates in our study were different from Salmonella Typhimurium isolates by the absence of three plasmid-borne genes (spvC, pefA, and rck) and the presence of gipA in all isolates. All Salmonella 1,4,[5],12:i:- isolates demonstrated MLST pattern ST34. Genomic deletions within the fljBA operon and surrounding genes were only found in Salmonella 1,4,[5],12:i:- isolates, with all isolates containing a deletion of fljB. However, hin and iroB were identified in all Salmonella 1,4,[5],12:i:- isolates. Three different deletion profiles were observed and two of them were different from the reported Salmonella 1,4,[5],12:i:- clones from Spain, America, and Italy, which provided some new evidence on the independent evolution of the multiple successful monophasic clones from Salmonella Typhimurium ancestors. This study is the first report of Salmonella 1,4,[5],12:i:- in food products from China. The data are more comprehensive and representative, providing valuable information for epidemiological studies, risk management, and public health strategies.
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