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      Antimicrobial resistance in clinical Escherichia coli isolates from poultry and livestock, China

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          Abstract

          Poultry and livestock are the most important reservoirs for pathogenic Escherichia coli and use of antimicrobials in animal farming is considered the most important factor promoting the emergence, selection and dissemination of antimicrobial-resistant microorganisms. The aim of our study was to investigate antimicrobial resistance in E. coli isolated from food animals in Jiangsu, China. The disc diffusion method was used to determine susceptibility to 18 antimicrobial agents in 862 clinical isolates collected from chickens, ducks, pigs, and cows between 2004 and 2012. Overall, 94% of the isolates showed resistance to at least one drug with 83% being resistance to at least three different classes of antimicrobials. The isolates from the different species were most commonly resistant to tetracycline, nalidixic acid, sulfamethoxazole, trimethoprim/sulfamethoxazole and ampicillin, and showed increasing resistance to amikacin, aztreonam, ceftazidime, cefotaxime, chloramphenicol, ciprofloxacin. They were least resistant to amoxicillin/clavulanic acid (3.4%) and ertapenem (0.2%). MDR was most common in isolates from ducks (44/44, 100%), followed by chickens (568/644, 88.2%), pigs (93/113, 82.3%) and cows (13/61, 21.3%). Our finding that clinical E. coli isolates from poultry and livestock are commonly resistant to multiple antibiotics should alert public health and veterinary authorities to limit and rationalize antimicrobial use in China.

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          Most cited references19

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          Public health. China takes aim at rampant antibiotic resistance.

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            The use and resistance to antibiotics in the community.

            The frequency of resistance to antibiotics among common community-acquired pathogens, and the number of drugs to which they are resistant have been increasing worldwide. The relationship between antibiotic usage and resistance is strongly supported by data from several studies. Countries with the highest per capita antibiotic consumption have the highest resistance. The emergence of penicillin-resistant Streptococcus pneumoniae is related to high consumption of antibiotics in general, as well as to increased use of aminopenicillins and/or probably to wider use of oral cephalosporins. Increased consumption of macrolides, especially the long-acting ones, correlates significantly with the level of macrolide resistance of group A streptococci and S. pneumoniae while increased use of oral cephalosporins might be associated with the increase of beta-lactamase-producing strains of Moraxella catarrhalis. Trimethoprim/sulphamethoxazole resistance is strongly associated with resistance to penicillin. A rise in consumption of fluoroquinolones is consonant with a higher rate of resistance to quinolones of S. pneumoniae, Escherichia coli and other Gram-negative bacteria. Paediatric bacterial isolates are more often resistant to various antimicrobial agents than isolates from adult patients; this higher resistance rate may be due to more frequent antimicrobial treatments in children, and extensive child to child transmission. Reliable data on antimicrobial consumption and resistance should form a basis for national policies devised to reduce the resistance of microorganisms to antibiotics.
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              Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland.

              Antimicrobial susceptibility testing was performed on a total of 581 clinical Escherichia coli isolates from diarrhea and edema disease in pigs, from acute mastitis in dairy cattle, from urinary tract infections in dogs and cats, and from septicemia in laying hens collected in Switzerland between 1999 and 2001. Among the 16 antimicrobial agents tested, resistance was most frequent for sulfonamides, tetracycline, and streptomycin. Isolates from swine presented significantly more resistance than those from the other animal species. The distribution of the resistance determinants for sulfonamides, tetracycline, and streptomycin was assessed by hybridization and PCR in resistant isolates. Significant differences in the distribution of resistance determinants for tetracycline (tetA, tetB) and sulfonamides (sulII) were observed between the isolates from swine and those from the other species. Resistance to sulfonamides could not be explained by known resistance mechanisms in more than a quarter of the sulfonamide-resistant and sulfonamide-intermediate isolates from swine, dogs and cats. This finding suggests that one or several new resistance mechanisms for sulfonamides may be widespread among E. coli isolates from these animal species. The integrase gene (intI) from class I integrons was detected in a large proportion of resistant isolates in association with the sulI and aadA genes, thus demonstrating the importance of integrons in the epidemiology of resistance in clinical E. coli isolates from animals.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Writing – original draft
                Role: Data curationRole: Methodology
                Role: ConceptualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Methodology
                Role: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Methodology
                Role: Data curationRole: Formal analysis
                Role: Data curationRole: Methodology
                Role: Formal analysisRole: Writing – original draft
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – original draft
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                21 September 2017
                2017
                : 12
                : 9
                : e0185326
                Affiliations
                [1 ] Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses; Yangzhou University College of Veterinary Medicine, Yangzhou, Jiangsu, PR China
                [2 ] Department of Food Hygiene and safety, Faculty of Public and Environmental Health, Khartoum University, Khartoum, Sudan
                [3 ] Poultry Institute, Chinese Academy of Agricultural Sciences, Yangzhou, Jiangsu, China
                [4 ] Department of Biomedical Sciences, Ross University School of Veterinary Medicine, Basseterre, St. Kitts, West Indies
                [5 ] Department of Diagnostic Medicine, Kansas State University, Manhattan, KS, United States of America
                [6 ] Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences Shanghai, China
                [7 ] Department of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL, United States of America
                Kansas State University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-7874-8340
                Article
                PONE-D-17-16853
                10.1371/journal.pone.0185326
                5608385
                28934348
                16594424-5049-4f0e-af55-add41c668b3e
                © 2017 Yassin et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 2 May 2017
                : 11 September 2017
                Page count
                Figures: 2, Tables: 1, Pages: 8
                Funding
                This project is funded by the National Key R & D Program of China (2016YFD0500804). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobial Resistance
                Medicine and Health Sciences
                Pharmacology
                Antimicrobial Resistance
                Biology and Life Sciences
                Agriculture
                Livestock
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobial Resistance
                Antibiotic Resistance
                Medicine and Health Sciences
                Pharmacology
                Antimicrobial Resistance
                Antibiotic Resistance
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Fowl
                Gamefowl
                Chickens
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Poultry
                Chickens
                Biology and Life Sciences
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                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Swine
                Biology and Life Sciences
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                Eukaryota
                Animals
                Vertebrates
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                Poultry
                Ducks
                Biology and Life Sciences
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                Ducks
                Medicine and Health Sciences
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                Biology and Life Sciences
                Microbiology
                Microbial Control
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                Research and Analysis Methods
                Experimental Organism Systems
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                Escherichia Coli
                Research and Analysis Methods
                Model Organisms
                Escherichia Coli
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Escherichia Coli
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
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