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      Prevalence, Antibiotic Susceptibility, and Molecular Characterization of Cronobacter spp. Isolated From Edible Mushrooms in China

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          Abstract

          Cronobacter spp. are foodborne pathogens that can infect and cause life-threatening diseases in all age groups, particularly in infants and immunocompromised elderly. This study aimed to investigate the prevalence, antibiotic susceptibility, and molecular characteristics of Cronobacter spp. isolates in edible mushrooms collected from 44 cities in China. In total, 668 edible mushrooms were collected from traditional retail markets and supermarkets and were analyzed by quantitative methods, PCR-based serotyping, multilocus sequence typing (MLST), and antibiotic susceptibility testing. Among the 668 samples tested, 89 (13.32%) were positive for Cronobacter spp., and the contamination levels exceeded the 110 most probable number (MPN)/g in 13.48% (12/89) of the samples. Flammulina velutipes samples had the highest contamination rate of 17.54% (37/211), whereas Hypsizygus marmoreus samples had the lowest contamination rate of 3.28% (2/61). Ten serotypes were identified among 115 isolates, of which the C. sakazakii serogroup O1 ( n = 32) was the primary serotype. MLST indicated that there was quite high genetic diversity in Cronobacter spp. and 72 sequence types were identified, 17 of which were new. Notably, C. sakazakii ST148 ( n = 10) was the most prevalent, followed by C. malonaticus ST7 ( n = 5). Antibiotic susceptibility testing revealed that the majority of Cronobacter spp. strains were susceptible to the 16 antibiotics tested. However, a portion of isolates exhibited relatively high resistance to cephalothin, with resistance and intermediate rates of 93.91 and 6.09%, respectively. One isolate (cro300A) was multidrug-resistant, with resistance to five antibiotics. Overall, this large-scale study revealed the relatively high prevalence and high genetic diversity of Cronobacter spp. on edible mushrooms in China, indicating a potential public health concern. To our knowledge, this is the first large-scale and systematic study on the prevalence of Cronobacter spp. on edible mushrooms in China, and the findings can provide valuable information that can guide the establishment of effective measures for the control and precaution of Cronobacter spp on edible mushrooms during production processes.

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          Most cited references49

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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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            Cronobacter spp. as emerging causes of healthcare-associated infection.

            Until recently, members of the Cronobacter genus (formerly known as Enterobacter sakazakii) were a relatively unknown cause of nosocomial infections. However, their association with infant infections, particularly through the consumption of contaminated reconstituted infant formula in neonatal intensive care units, has resulted in international efforts to improve neonatal health care. To investigate current understanding of this emergent group of bacterial pathogens and the steps taken to reduce neonatal infection. A literature review was undertaken to determine current knowledge of the Cronobacter genus with respect to recent taxonomic revisions, sources and clinical relevance. The majority of severe neonatal meningitis infections are associated with one of the 10 Cronobacter spp., the clonal complex known as C. sakazakii sequence type 4. International efforts by the Food and Agriculture Organization-World Health Organization (WHO) to reduce the risk of neonatal infection by this organism have resulted in improved microbiological safety of powdered infant formula (PIF), but revised guidelines for feeding practices have been problematic. In addition, the majority of infections occur in the adult population and the sources are unknown. International improvements in the microbiological safety of PIF and advice on feeding practices have focused on improving neonatal health care following the heightened awareness of Cronobacter infections in this particular age group. These measures are also likely to reduce neonatal exposure to other opportunistic bacterial pathogens, but a number of unresolved issues remain with respect to the practicalities of feeding premature neonates safely while following WHO advice. Copyright © 2013 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.
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              Enterobacter sakazakii infections among neonates, infants, children, and adults. Case reports and a review of the literature.

              Samuel Lai (2001)
              Enterobacter sakazakii can cause serious infections especially among the very young and the elderly. It continues to be more common among neonates and infants than adults. Its tropism for the central nervous system in neonates and infants remains a mystery. Among neonates and infants, E. sakazakii has a propensity to cause meningitis resulting in ventriculitis, brain abscess or cyst formation, and development of hydrocephalus requiring ventricular-peritoneal shunt. Computed tomography of the head is therefore useful in following patients with E. sakazakii meningitis. Mortality and morbidity of E. sakazakii meningitis is high, and virtually all patients recovering from the central nervous system infection suffered mental and physical developmental delays. The case-fatality rate decreased among patients with meningitis treated with the third-generation cephalosporins. Most adults with E. sakazakii infection had serious underlying diseases and 50% of the adults with the infection had malignancies. However there has never been a known case of meningitis. Increasing antibiotic resistance among Enterobacter species should lead one to consider using the carbapenems or the newer cephalosporins in combination with a second agent such as an aminoglycoside. Limited data suggest that trimethoprim-sulfamethoxazole may be a useful agent in the treatment of infections caused by the Enterobacter species, especially in view of the production of extended-spectrum beta-lactamases capable of inactivating the cephalosporins and extended-spectrum penicillin.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                26 February 2019
                2019
                : 10
                : 283
                Affiliations
                [1] 1State 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
                [2] 2Department of Food Science and Technology, Jinan University , Guangzhou, China
                [3] 3College of Food Science, South China Agricultural University , Guangzhou, China
                Author notes

                Edited by: Julio Parra-Flores, University of the Bío-Bío, Chile

                Reviewed by: Juan Aguirre, Universidad de Chile, Chile; Elba Veronica Arias Rios, IEH Laboratories and Consulting Group, United States

                *Correspondence: Qingping Wu wuqp203@ 123456163.com

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

                †These authors have contributed equally to this work

                Article
                10.3389/fmicb.2019.00283
                6399401
                6ffaadbd-6978-49c7-ace2-d9301c23142e
                Copyright © 2019 Li, Zeng, Zhang, He, Ling, Chen, Wu, Lei, Wu, Ye, Ding, Wang, Wei, Zhang and Wu.

                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(s) 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.

                History
                : 30 October 2018
                : 04 February 2019
                Page count
                Figures: 2, Tables: 3, Equations: 0, References: 55, Pages: 9, Words: 6171
                Funding
                Funded by: National Key R&D Program of China
                Award ID: 2017YFC1601200
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31601571
                Funded by: Local Innovative and Research Teams Project of Guangdong PEARL River Talents Program
                Award ID: 2017BT01S174
                Funded by: Pearl River S&T Nova Program of Guangzhou 10.13039/501100009334
                Award ID: 201806010062
                Funded by: GDAS' Special Project of Science and Technology Development
                Award ID: 2017GDASCX-0201
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                cronobacter,prevalence,edible mushrooms,multilocus sequence typing,o-antigen serotyping,antibiotic susceptibility test

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