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      Antimicrobial resistance in Enterobacteriaceae from healthy broilers in Egypt: emergence of colistin-resistant and extended-spectrum β-lactamase-producing Escherichia coli

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          Abstract

          Background

          Poultry remains one of the most important reservoir for zoonotic multidrug resistant pathogens. The global rise of antimicrobial resistance in Gram-negative bacteria is of reasonable concern and demands intensified surveillance.

          Methods

          In 2016, 576 cloacal swabs were collected from 48 broiler farms located in five governorates in northern Egypt. Isolates of Enterobacteriaceae could be cultivated on different media and were identified by MALDI-TOF MS and PCR. Escherichia coli isolates were genotyped by DNA-microarray-based assays. The antimicrobial susceptibility to 14 antibiotics was determined and resistance-associated genes were detected. The VITEK-2 system was applied for phenotypical confirmation of extended-spectrum β-lactamase-producing isolates. The determination of colistin resistance was carried out phenotypically using E-test and genotypically using PCR for detection of the mcr-1 gene.

          Results

          Out of 576 samples, 72 representatives of Enterobacteriaceae were isolated and identified as 63 E. coli (87.5%), 5 Enterobacter cloacae (6.9%), 2 Klebsiella pneumoniae (2.8%) and 2 Citrobacter spp. (2.8%). Seven out of 56 cultivated E. coli (12.5%) were confirmed as ESBL-producing E. coli and one isolate (1.8%) as ESBL/carbapenemase-producing E. coli. Five out of 63 E. coli isolates (7.9%) recovered from different poultry flocks were phenotypically resistant to colistin and harboured mcr-1 gene.

          Conclusions

          This is the first study reporting colistin resistance and emergence of multidrug resistance in Enterobacteriaceae isolated from healthy broilers in the Nile Delta region, Egypt. Colistin-resistant E. coli in poultry is of public health significance. The global rise of ESBL- and carbapenemase-producing Gram-negative bacteria demands intensified surveillance. ESBL-producing E. coli in poultry farms in Egypt are of major concern that emphasizes the possibility of spread of such strains to humans. The results also reinforce the need to develop strategies and to implement specific control procedures to reduce the use of antibiotics.

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          Most cited references67

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          Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe.

          Plasmid-acquired carbapenemases in Enterobacteriaceae, which were first discovered in Europe in the 1990s, are now increasingly being identified at an alarming rate. Although their hydrolysis spectrum may vary, they hydrolyse most β-lactams, including carbapenems. They are mostly of the KPC, VIM, NDM and OXA-48 types. Their prevalence in Europe as reported in 2011 varies significantly from high (Greece and Italy) to low (Nordic countries). The types of carbapenemase vary among countries, partially depending on the cultural/population exchange relationship between the European countries and the possible reservoirs of each carbapenemase. Carbapenemase producers are mainly identified among Klebsiella pneumoniae and Escherichia coli, and still mostly in hospital settings and rarely in the community. Although important nosocomial outbreaks with carbapenemase-producing Enterobacteriaceae have been extensively reported, many new cases are still related to importation from a foreign country. Rapid identification of colonized or infected patients and screening of carriers is possible, and will probably be effective for prevention of a scenario of endemicity, as now reported for extended-spectrum β-lactamase (mainly CTX-M) producers in all European countries. © 2012 The Authors. Clinical Microbiology and Infection © 2012 European Society of Clinical Microbiology and Infectious Diseases.
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            CTX-M: changing the face of ESBLs in Europe.

            Since around 2000 - earlier in Poland and Spain and later in France and the UK - dramatic shifts have occurred in the prevalence and types of extended-spectrum beta-lactamases (ESBLs) in Europe. Before this watershed, most producers were nosocomial isolates, often Klebsiella spp. or Enterobacter spp. from specialist care units, and had mutant TEM or SHV ESBLs. Subsequently, CTX-M ESBLs have become dominant, with much greater penetration into Escherichia coli, and with many infections in 'complicated community' patients, usually with underlying disease, recent antibiotic usage, or healthcare contact. The degree of clonality among producers varies with the country, as does the enzyme type produced, with group 9 (CTX-M-9 and -14) enzymes dominant in Spain and group 1 enzymes (particularly CTX-M-3 and -15) dominant elsewhere. Irrespective of the particular enzyme, most producers are multiresistant. These changing patterns present major therapeutic and infection control challenges, with the public health intervention points unclear.
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              Extended-spectrum β-lactamases in Gram Negative Bacteria

              Extended-spectrum β-lactamases (ESBLs) are a group of plasmid-mediated, diverse, complex and rapidly evolving enzymes that are posing a major therapeutic challenge today in the treatment of hospitalized and community-based patients. Infections due to ESBL producers range from uncomplicated urinary tract infections to life-threatening sepsis. Derived from the older TEM is derived from Temoniera, a patient from whom the strain was first isolated in Greece. β-lactamases, these enzymes share the ability to hydrolyze third-generation cephalosporins and aztreonam and yet are inhibited by clavulanic acid. In addition, ESBL-producing organisms exhibit co-resistance to many other classes of antibiotics, resulting in limitation of therapeutic option. Because of inoculum effect and substrate specificity, their detection is also a major challenge. At present, however, organizations such as the Clinical and Laboratory Standards Institute (formerly the National Committee for Clinical Laboratory Standards) provide guidelines for the detection of ESBLs in Klebsiella pneumoniae, K. oxytoca, Escherichia coli and Proteus mirabilis. In common to all ESBL-detection methods is the general principle that the activity of extended-spectrum cephalosporins against ESBL-producing organisms will be enhanced by the presence of clavulanic acid. Carbapenems are the treatment of choice for serious infections due to ESBL-producing organisms, yet carbapenem-resistant isolates have recently been reported. ESBLs represent an impressive example of the ability of gram-negative bacteria to develop new antibiotic-resistance mechanisms in the face of the introduction of new antimicrobial agents. Thus there is need for efficient infection-control practices for containment of outbreaks; and intervention strategies, e.g., antibiotic rotation to reduce further selection and spread of these increasingly resistant pathogens.
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                Author and article information

                Contributors
                +49-36418042249 , amira.moawad@fli.de
                +49-36418042249 , hosny.eladawy@fli.de
                Journal
                Gut Pathog
                Gut Pathog
                Gut Pathogens
                BioMed Central (London )
                1757-4749
                19 September 2018
                19 September 2018
                2018
                : 10
                : 39
                Affiliations
                [1 ]Friedrich-Loeffler-Institut (Federal Research Institute for Animal Health), Institute of Bacterial Infections and Zoonoses, Naumburger Str. 96a, 07743 Jena, Germany
                [2 ]Provincial Laboratory, Institute of Animal Health Research, Mansoura, Egypt
                [3 ]ISNI 0000 0000 9116 4836, GRID grid.14095.39, Institute for Poultry Diseases, , Free University Berlin, ; Königsweg 63, 14163 Berlin, Germany
                [4 ]ISNI 0000 0004 0539 6243, GRID grid.472845.8, Alere Technologies GmbH, ; Löbstedter Str. 103-105, 07749 Jena, Germany
                [5 ]InfectoGnostics Research Campus Jena e. V., Philosophenweg 7, 07743 Jena, Germany
                [6 ]ISNI 0000 0001 2111 7257, GRID grid.4488.0, Institute for Medical Microbiology and Hygiene, Medical Faculty Carl Gustav Carus, , Technische Universität Dresden, ; Fetscherstr. 74, 01307 Dresden, Germany
                [7 ]ISNI 0000 0000 9116 4836, GRID grid.14095.39, Institute for Animal Hygiene and Environmental Health, , Free University Berlin, ; Robert-von Ostertag-Str. 7-13, 14163 Berlin, Germany
                [8 ]ISNI 0000 0004 0578 3577, GRID grid.411978.2, Faculty of Veterinary Medicine, , Kafrelsheikh University, ; Kafr El-Sheikh, 33516 Egypt
                Author information
                http://orcid.org/0000-0002-8585-4237
                Article
                266
                10.1186/s13099-018-0266-5
                6148799
                30250514
                d30ac846-d972-4a03-a6ec-3c108bdfec3e
                © The Author(s) 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 29 May 2018
                : 12 September 2018
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Gastroenterology & Hepatology
                enterobacteriaceae,antibiotic resistance,dna microarray,esbl,colistin,broiler

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