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      Prevalence and Molecular and Antimicrobial Characteristics of Cronobacter spp. Isolated From Raw Vegetables in China


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          Cronobacter spp. is a foodborne pathogen that causes life-threatening and invasive diseases, such as necrotizing enterocolitis, meningitis, and sepsis. In this study, we aimed to investigate the prevalence, molecular characteristics and antimicrobial resistance of Cronobacter spp. in raw vegetables marketed in China. Based on dietary habits in China, 403 raw vegetables that could be eaten without additional cooking were collected. Of the 403 samples tested, 122 (30.27%) were positive for Cronobacter spp., and the contamination levels exceeded 110 most probable number (MPN)/g for 16.39% (20/122) of the samples. Coriander samples had the highest contamination rate of 52.81%, and the MPN values of 19.15% of positive coriander samples exceeded 100 MPN/g. Eleven serotypes were identified among 171 isolates, with Cronobacter sakazakii serogroup O1 (41 isolates) being the dominant serotype. Molecular characterization indicated that there was quite high genetic diversity in Cronobacter spp., and multilocus sequence typing analyses yielded 106 sequence types (STs), 55 of which were newly identified. Notably, the most prevalent ST (eight isolates) was C. malonaticus ST60, which appeared in a recent clinical infectious disease study in China. Five C. sakazakii ST4, seven C. malonaticus ST7, and three C. sakazakii ST8 confirmed as pathogenic STs in other countries were also detected in this study. Furthermore, all isolates were susceptible to amikacin, amoxicillin-clavulanic, cefepime, ciprofloxacin, and imipenem, but some isolates exhibited a high ratio of resistance to cephalothin (59.65%). In this study, the high contamination rate and the detection of pathogenic and new STs in raw vegetables indicated potential hazards to customers. To the best of our knowledge, this is the first report to provide valuable information on the contamination status of Cronobacter spp. in vegetables that can be eaten raw in China.

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          Most cited references 52

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          Cronobacter gen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov., comb. nov., Cronobacter malonaticus sp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies, Cronobacter dublinensis subsp. dublinensis subsp. nov., Cronobacter dublinensis subsp. lausannensis subsp. nov. and Cronobacter dublinensis subsp. lactaridi subsp. nov.

          [Enterobacter] sakazakii is an opportunistic pathogen that can cause infections in neonates. This study further clarifies the taxonomy of isolates described as [E.] sakazakii and completes the formal description of the proposed reclassification of these organisms as novel species and subspecies within a proposed novel genus, Cronobacter gen. nov. [E.] sakazakii was first defined in 1980, however recent polyphasic taxonomic analysis has determined that this group of organisms consists of several genomospecies. In this study, the phenotypic descriptions of the proposed novel species are expanded using Biotype 100 and Biolog Phenotype MicroArray data. Further DNA-DNA hybridization experiments showed that malonate-positive strains within the [E.] sakazakii genomospecies represent a distinct species, not a subspecies. DNA-DNA hybridizations also determined that phenotypically different strains within the proposed species, Cronobacter dublinensis sp. nov., belong to the same species and can be considered as novel subspecies. Based on these analyses, the following alternative classifications are proposed: Cronobacter sakazakii gen. nov., comb. nov. [type strain ATCC 29544(T) (=NCTC 11467(T))]; Cronobacter malonaticus sp. nov. [type strain CDC 1058-77(T) (=LMG 23826(T)=DSM 18702(T))]; Cronobacter turicensis sp. nov. [type strain z3032(T) (=LMG 23827(T)=DSM 18703(T))]; Cronobacter muytjensii sp. nov. [type strain ATCC 51329(T) (=CIP 103581(T))]; Cronobacter dublinensis sp. nov. [type strain DES187(T) (=LMG 23823(T)=DSM 18705(T))]; Cronobacter dublinensis subsp. dublinensis subsp. nov. [type strain DES187(T) (=LMG 23823(T)=DSM 18705(T))]; Cronobacter dublinensis subsp. lausannensis subsp. nov. [type strain E515(T) (=LMG 23824=DSM 18706(T))], and Cronobacter dublinensis subsp. lactaridi subsp. nov. [type strain E464(T) (=LMG 23825(T)=DSM 18707(T))].
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            Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula.

            We describe an outbreak of necrotizing enterocolitis (NEC) that occurred in the neonatal intensive care unit of our hospital. A total of 12 neonates developed NEC in June-July 1998. For two of them, twin brothers, the NEC turned out to be fatal. Enterobacter sakazakii, a known contaminant of powdered milk formula, was isolated from a stomach aspirate, anal swab, and/or blood sample for 6 of the 12 neonates. A review of feeding procedures revealed that 10 of the 12 patients were fed orally with the same brand of powdered milk formula. E. sakazakii was isolated from the implicated prepared formula milk as well as from several unopened cans of a single batch. Molecular typing by arbitrarily primed PCR (AP-PCR) confirmed, although partially, strain similarity between milk and patient isolates. No further cases of NEC were observed after the use of the contaminated milk formula was stopped. With this outbreak we show that intrinsic microbiological contamination of powdered milk formula can be a possible contributive factor in the development of NEC, a condition encountered almost exclusively in formula-fed premature infants. The use of sterilized liquid milk formula in neonatal care could prevent problems with intrinsic and extrinsic contamination of powdered milk formula.
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              Modes and modulations of antibiotic resistance gene expression.

              Since antibiotic resistance usually affords a gain of function, there is an associated biological cost resulting in a loss of fitness of the bacterial host. Considering that antibiotic resistance is most often only transiently advantageous to bacteria, an efficient and elegant way for them to escape the lethal action of drugs is the alteration of resistance gene expression. It appears that expression of bacterial resistance to antibiotics is frequently regulated, which indicates that modulation of gene expression probably reflects a good compromise between energy saving and adjustment to a rapidly evolving environment. Modulation of gene expression can occur at the transcriptional or translational level following mutations or the movement of mobile genetic elements and may involve induction by the antibiotic. In the latter case, the antibiotic can have a triple activity: as an antibacterial agent, as an inducer of resistance to itself, and as an inducer of the dissemination of resistance determinants. We will review certain mechanisms, all reversible, that bacteria have elaborated to achieve antibiotic resistance by the fine-tuning of the expression of genetic information.

                Author and article information

                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                05 June 2018
                : 9
                1School of Bioscience and Bioengineering, South China University of Technology , Guangzhou, China
                2State Key Laboratory of Applied Microbiology, South China, Guangdong Provincial Key Laboratory of Microbiology Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangdong Institute of Microbiology , Guangzhou, China
                3College of Food Science, South China Agricultural University , Guangzhou, China
                4Department of Food Science & Technology, Jinan University , Guangzhou, China
                Author notes

                Edited by: Michael Gänzle, University of Alberta, Canada

                Reviewed by: Vijay K. Juneja, United States Department of Agriculture, United States; Magaly Toro, Universidad de Chile, Chile

                *Correspondence: Qingping Wu, wuqp203@ 123456163.com ; wuqp@ 123456gdim.cn

                These authors have contributed equally to this work.

                This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

                Copyright © 2018 Ling, Li, Zhang, Wu, Zeng, He, Ye, Wang, Ding, Chen, Xue, Ye and Guo.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

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                Figures: 3, Tables: 5, Equations: 0, References: 58, Pages: 10, Words: 0
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