Shenghui Cui

Prevalence and characterization of Salmonella serovars in retail meats of marketplace in Shaanxi, China

A total of 764 retail meat including 515 chicken, 91 pork, 78 beef and 80 lamb samples were collected in Shaanxi Province of China in 2007-2008 to determine the prevalence of Salmonella. The isolates were characterized using serotyping, antimicrobial susceptibility testing, and the presence of bla(CMY-2) and bla(TEM) and class I integrons. Selective serovars were further subtyped using PFGE. Approximately 54% (276) of chicken, 31% (28) of pork, 17% (13) of beef and 20% (16) of lamb samples were positive of Salmonella. Among 24 serovars identified, Enteritidis (31.5%) was most common, followed by Typhimurium (13.4%), Shubra (10.0%), Indiana (9.7%), Derby (9.5%) and Djugu (7.0%). Nearly 80% of the isolates (283) were resistant to at least one antimicrobial, and 53% (191) to more than three antimicrobials. Resistance was most frequently observed to sulfamethoxazole (67%), to trimethoprim/sulfamethoxazole (58%) and to tetracycline (56%). Furthermore, many isolates were resistant to nalidixic acid (35%), ciprofloxacin (21%) and ceftriaxone (16%). Most isolates of Shubra (89%) and Indiana (88%) were resistant to > or = 9 antimicrobials, compared to only 11% of Enteritidis and 9% of Infantis that showed similar resistance. Class I integrons were detected in 10% of the isolates, and contained aadA, tetR, dhfr, bla(PSE-1), bla(DHA-1) and bla(VEB-1) gene cassettes alone or various combinations. Ceftriaxone- and/or cefoperazone-resistant isolates (n=62) carried bla(TEM) (51.6%) and/or bla(CMY-2) (56.5%). A total of 116 PFGE patterns were generated among 210 selected isolates. Our findings indicated that Salmonella contamination was common in retail meats, and that the Salmonella isolates were phenotypically and genetically diverse. Additionally, many Salmonella isolates were resistant to multiple antimicrobials.

Prevalence of Salmonella on Raw Poultry at Retail Markets in China

Data regarding Salmonella on raw poultry are very limited in China. The objective of this study was to determine the prevalence of Salmonella on raw poultry at the retail level in six provinces and two national cities in China. Whole chicken carcasses (n = 1,152) were collected from three types of retail markets (large, small, and wet). All samples were analyzed for the presence of Salmonella by using the U.S. Department of Agriculture, Food Safety Inspection Service method. Of 1,152 chicken samples, overall Salmonella prevalence was 52.2%. The highest prevalence was observed in Guangxi Province (65.3%), next in Guangdong Province (64.6%), and then in Beijing (63.9%), Shaanxi Province (50.7%), Henan Province (47.9%), Shanghai (44.4%), and Fujian Province (42.4%), and lowest prevalence was observed in Sichuan Province (38.9%). Salmonella prevalence was significantly different among the six provinces and two national cities. Salmonella prevalence was highest in the wet markets (54.4%) compared with the large markets (50.3%) and the small markets (52.1%), but differences were not significant (P > 0.05). Good manufacturing practices, good agricultural practices, and hazard analysis critical control point systems for Salmonella control in poultry production at the farm, processing, and retail level should be implemented.

Prevalence and quantitative detection of Salmonella in retail raw chicken in Shaanxi, China.

Quantitative Salmonella concentrations and prevalence of Salmonella in raw chicken at the retail level in Shaanxi province, China, was determined in this study. Two hundred forty samples were collected in Yangling and the surrounding cities, in Shaanxi Province, China, for data collection over 12 successive months from April 2011 to March 2012. During the whole surveillance year, the overall Salmonella contamination rate of retail raw chicken was identified as 43.3%, the most-probable-number (MPN) values ranged from 0.0036 to 0.8596 MPN per g, and the average value was 0.1655 MPN per g, except in 11 of the samples, which had MPN values of more than 11 MPN per g. In April 2011, the highest prevalence rate, which was 80.0%, was observed, and the corresponding MPN value was 0.8596 MPN per g. Observed in November 2011, the lowest prevalence rate and the corresponding MPN value were 5.0% and 0.0036 MPN per g, respectively. Prevalence of Salmonella in chicken collected from the supermarket (49.2%) was higher but not significantly different from that in the wet markets (37.5%), although the MPN value of samples in the wet market (0.1912 MPN per g) was higher than that in the supermarket (0.1396 MPN per g). Prevalence of Salmonella was the highest in the frozen chicken (53.3%) compared with chilled chicken (45.0%) and freshly slaughtered chicken (37.5%); however, the MPN value of the freshly slaughtered chicken (0.1912 MPN per g) was higher than those of either frozen chicken (0.1804 MPN per g) or the chilled chicken (0.0988 MPN per g).

Characterization of extended-spectrum β-lactamases (ESBLs)-producing Salmonella in retail raw chicken carcasses

Extended-spectrum β-lactamases (ESBLs)-producing Salmonella is considered a serious concern to public health worldwide. However, limited information is available on ESBLs-producing Salmonella in retail chicken products in China. The objective of this study was to characterize ESBLs-producing Salmonella isolates from retail chickens in China. A total of 890 Salmonella isolates from retail chicken carcasses collected from 4 provinces were firstly screened for ESBLs-production phenotype via the double-disk synergy test method. A total of 96 (10.8%, n=890) ESBLs-producing Salmonella were identified and subjected to PFGE analysis, characterization for the presence of ESBLs encoding genes, transposons, carbapenemase and virulence genes. A total of 59 PFGE profiles were detected in these 96 isolates, among which 57.3% were found to harbor blaTEM-1, whereas 30.2%, 24.0%, 18.8% and 7.3% were carrying blaOXA-1, blaCTX-M-15, blaCTX-M-3 and blaPSE-1 genes, respectively. Moreover, 42 (43.8%) isolates co-carried 2 ESBLs-producing genes, and two (2.1%) isolates co-carried 3 genes. Furthermore, 24 (25.0%) ESBLs-producing isolates carried VIM and 10 (10.4%) carried KPC encoding genes that closely associated with carbapenems resistance. Eighty-eight isolates harbored transposons ranging from 4.2% for Tn903 to 76.0% for Tn21. Out of the 88 Salmonella that harbored transposons, 25%, 22.7%, 23.9%, 10.2% and 1.1% of isolates were found to carry 2, 3, 4, 5 and 6 transposons, respectively. The minimum inhibitory concentration (MIC) values for cephalosporins (ceftriaxone, cefoperazone and cefoxitin) to ESBLs-producing isolates were from 4 to 1024μg/mL, for nalidixic acid were from 64 to 512μg/mL, for fluoroquinolones (ciprofloxacin, levofloxacin and gatifloxacin) were from 4 to 256μg/mL. Twenty-nine virulence genes were detected in the 96 ESBLs-producing isolates with 2.1% harbored spvR (lowest) and 90.6% harbored marT and steB (highest). All isolates carried at least one virulence gene, 83.3% of the isolates co-carried ≥10, 17.7% co-carried ≥15, and 1.0% co-carried 23 virulence genes. Interestingly, 16.7% of the isolates resistant to >12 antibiotics tested and shown to carry >4 transposons and 10 virulence genes. Our findings indicated that ESBLs-producing Salmonella isolated from retail chicken meat in China were highly resistant to antibiotics, frequently harbored transposons, virulence genes, carbapenems hydrolysis enzymes and ESBLs encoding genes. These isolates can pose a significant public health risk.

Emergence of β-Lactamases and Extended-Spectrum β-Lactamases (ESBLs) Producing Salmonella in Retail Raw Chicken in China

β-Lactamases and extended-spectrum β-lactamases (ESBLs) producing pathogenic bacteria were widely studied previously in China, but were seldom focused on foodborne Salmonella. In this study, an investigation concerning β-lactamases and ESBLs producing Salmonella recovered from retail raw chickens was performed. Sixty of 699 foodborne Salmonella isolates were detected as β-lactamases and ESBLs-producing ones that covered 12 Salmonella serotypes and exhibited different pulsed-field gel electrophoresis genotypes. Forty-four of 60 β-lactamases and ESBLs-producing strains were simultaneously resistant to ampicillin, amoxicillin/clavulanic acid, ceftiofur, ceftriaxone, and cefoxitin. The most commonly detected β-lactamases and ESBLs-encoding gene was bla(TEM-1) (n = 44), followed by bla(OXA-1) (n = 38), bla(CMY-2) (n = 29), bla(PSE-1-like) (n = 1), bla(CTX-M-3) (n = 16), and bla(CTX-M-15) (n = 1), respectively. Fourteen, 24, 21, and 1 isolates were detected simultaneously positive for 1, 2, 3, and 4 of the detected β-lactamases and ESBLs-encoding genes, respectively. A Salmonella strain simultaneously co-carrying bla(TEM-1), bla(OXA-1), bla(CMY-2), and bla(CTX-M-3) was first reported in the present study. Amino acid substitution of Trp244Cys/His247Leu was detected in PSE-1, Val218Asp in CMY-2, and Asp242Gly in CTX-M-15 enzymes, respectively. A difference was found among the amino acid sequences of the detected OXA-1, CMY-2, CTX-M, PSE-1, and TEM-1. The results demonstrated that β-lactamases and ESBLs were emerging and prevalent in foodborne Salmonella.