Abstract
In this study, we characterized the β-lactamase genes and phenotypic resistance of cephalosporin-resistant Enterobacteriaceae isolated from retail foods in China. Of 1,024 Enterobacteriaceae isolates recovered from raw meat products, aquatic products, raw vegetables, retail-level ready-to-eat (RTE) foods, frozen foods, and mushrooms from 2011 to 2014, 164 (16.0%) showed cefotaxime (CTX) and/or ceftazidime (CAZ) cephalosporin resistance, and 96 (9.4%) showed the extended-spectrum β-lactamase (ESBL) phenotype. More than 30% isolates were resistant to all antimicrobial agents except carbapenems (MEM 3.1% and IPM 5.2%), cefoxitin (FOX 6.3%), and amoxicillin/clavulanic acid (AMC 26%), and 94.8% of the strains were resistant to up to seven antibiotics. Polymerase chain reaction analysis showed that blaTEM (81.9%) was the most common gene, followed by blaCTX-M (68.1%) and blaSHV (38.9%). Moreover, 16.8% (72/429) of food samples contained ESBL-positive Enterobacteriaceae, with the following patterns: 32.9% (23/70) in frozen foods, 27.2% (5/29) in mushrooms, 17.6% (24/131) in raw meats, 13.3% (4/30) in fresh vegetables, 11.1% (8/72) in RTE foods, and 9.3% (9/97) in aquatic products. In addition, 24 of 217 foods collected in South China (11.1%), 25 of 131 foods collected in North of the Yangtze River region (19.1%), and 23 of 81 foods collected in South of the Yangtze River region (28.4%) were positive for ESBL- Enterobacteriaceae. Conjugation experiments demonstrated that the 22 of 72 isolates were transconjugants that had received the β-lactamase gene and were resistant to β-lactam antibiotics as well as some non-β-lactam antibiotics. These findings demonstrated that retail foods may be reservoirs for the dissemination of β-lactam antibiotics and that resistance genes could be transmitted to humans through the food chain; and the predominant ESBL-producing Enterobacteriaceae in China was isolated from in frozen chicken-meat, followed by frozen pork, cold noodles in sauce, cucumber, raw chicken meat, frozen pasta, brine-soaked chicken and tomato.
Highlights
Enterobacteriaceae, a large family of gram-negative, nonspore-forming, rod-shaped, facultative anaerobes capable of fermenting sugars to various end products, are important hygiene indicators for process verification in food production, recently replacing the poorly defined group of coliforms (Anonymous, 2005)
For isolation of Salmonella, 25 g food sample was pre-enriched in 225 ml of buffered peptone broth (Huankai); one milliliter cultures were incubated in 10 ml of selenite cystine broth (SC) (Huankai) at 37◦C and 10 ml of tetrathionate brilliant green broth (TTB) at 42◦C for 24 h, respectively; loopfuls of SC and TTB cultures were streaked onto xyloselysine-tergitol 4 (XLT4) selective agar plates (Difco, Detroit, MI, USA) and chromogenic Salmonella agar plates (Huankai), incubated at 37◦C for 24 h; presumptive colonies were picked from each plate, stabbed into a triple sugar iron slant (Huankai), and incubated at 37◦C for 24 h; isolates with typical Salmonella phenotypes were further confirmed using API 20E test strips (BioMe′rieux, Marcy I′Etoile, France)
The remaining strains were identified as Citrobacter freundii, C. koseri, C. amalonaticus, and Serratia marcescens
Summary
Enterobacteriaceae, a large family of gram-negative, nonspore-forming, rod-shaped, facultative anaerobes capable of fermenting sugars to various end products, are important hygiene indicators for process verification in food production, recently replacing the poorly defined group of coliforms (Anonymous, 2005). Beta-lactams (mainly extended-spectrum cephalosporins and carbapenems) and fluoroquinolones are the primary therapeutic choices to treat infections caused by Enterobacteriaceae (Bassetti et al, 2015) Resistance to these antimicrobials has been increasing in recent years (Ben Sallem et al, 2012; Blaak et al, 2014; Durso and Cook, 2014)
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