Antimicrobial Resistance Profiles and Macrolide Resistance Mechanisms of <i>Campylobacter coli</i> Isolated from Pigs and Chickens

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Abstract

We identified 1218 Campylobacter coli isolates from fecal and carcass samples of pigs ( n = 643) and chickens ( n = 575) between 2010 and 2018. About 99% of the isolates were resistant to at least one antimicrobial agent. The isolates exhibited high resistance rates (>75%) to ciprofloxacin, nalidixic acid, and tetracycline. Azithromycin and erythromycin resistance rates were the highest in isolates from pigs (39.7% and 39.2%, respectively) compared to those of chickens (15.8% and 16.3%, respectively). Additionally, a low-to-moderate proportion of the isolates were resistant to florfenicol, gentamicin, clindamycin, and telithromycin. Multidrug resistance (MDR) was found in 83.1% of the isolates, and profiles of MDR usually included ciprofloxacin, nalidixic acid, and tetracycline. We found point mutation (A2075G) in domain V of the 23S rRNA gene in the majority of erythromycin-resistant isolates. Multilocus sequence typing of 137 erythromycin-resistant C. coli isolates revealed 37 previously reported sequence types (STs) and 8 novel STs. M192I, A103VI, and G74A substitutions were frequently noted in the ribosomal proteins L4 or L22. Further, we identified a considerable proportion (>90%) of erythromycin-resistant isolates carrying virulence factor genes: flaA, cadF, ceuE, and VirB. The prudent use of antimicrobials and regular microbiological investigation in food animals will be vital in limiting the public health hazards of C. coli in Korea.

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Most cited references 64

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Multilocus sequence typing system for Campylobacter jejuni.

K Dingle, F. Colles, D Wareing … (2001)

The gram-negative bacterium Campylobacter jejuni has extensive reservoirs in livestock and the environment and is a frequent cause of gastroenteritis in humans. To date, the lack of (i) methods suitable for population genetic analysis and (ii) a universally accepted nomenclature has hindered studies of the epidemiology and population biology of this organism. Here, a multilocus sequence typing (MLST) system for this organism is described, which exploits the genetic variation present in seven housekeeping loci to determine the genetic relationships among isolates. The MLST system was established using 194 C. jejuni isolates of diverse origins, from humans, animals, and the environment. The allelic profiles, or sequence types (STs), of these isolates were deposited on the Internet (http://mlst.zoo.ox.ac.uk), forming a virtual isolate collection which could be continually expanded. These data indicated that C. jejuni is genetically diverse, with a weakly clonal population structure, and that intra- and interspecies horizontal genetic exchange was common. Of the 155 STs observed, 51 (26% of the isolate collection) were unique, with the remainder of the collection being categorized into 11 lineages or clonal complexes of related STs with between 2 and 56 members. In some cases membership in a given lineage or ST correlated with the possession of a particular Penner HS serotype. Application of this approach to further isolate collections will enable an integrated global picture of C. jejuni epidemiology to be established and will permit more detailed studies of the population genetics of this organism.

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The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017

(2019)

Abstract The data on antimicrobial resistance in zoonotic and indicator bacteria in 2017, submitted by 28 EU Member States (MSs), were jointly analysed by EFSA and ECDC. Resistance in zoonotic Salmonella and Campylobacter from humans, animals and food, and resistance in indicator Escherichia coli as well as meticillin‐resistant Staphylococcus aureus in animals and food were addressed, and temporal trends assessed. ‘Microbiological’ resistance was assessed using epidemiological cut‐off (ECOFF) values; for some countries, qualitative data on human isolates were interpreted in a way which corresponds closely to the ECOFF‐defined ‘microbiological’ resistance. In Salmonella from humans, as well as in Salmonella and E. coli isolates from fattening pigs and calves of less than 1 year of age, high proportions of isolates were resistant to ampicillin, sulfonamides and tetracyclines, whereas resistance to third‐generation cephalosporins was uncommon. Varying occurrence/prevalence rates of presumptive extended‐spectrum beta‐lactamase (ESBL)/AmpC producers in Salmonella and E. coli monitored in meat (pork and beef), fattening pigs and calves, and Salmonella monitored in humans, were observed between countries. Carbapenemase‐producing E. coli were detected in one single sample from fattening pigs in one MS. Resistance to colistin was observed at low levels in Salmonella and E. coli from fattening pigs and calves and meat thereof and in Salmonella from humans. In Campylobacter from humans, high to extremely high proportions of isolates were resistant to ciprofloxacin and tetracyclines, particularly in Campylobacter coli. In five countries, high to very high proportions of C. coli from humans were resistant also to erythromycin, leaving few options for treatment of severe Campylobacter infections. High resistance to ciprofloxacin and tetracyclines was observed in C. coli isolates from fattening pigs, whereas much lower levels were recorded for erythromycin. Combined resistance to critically important antimicrobials in both human and animal isolates was generally uncommon but very high to extremely high multidrug resistance levels were observed in S. Typhimurium and its monophasic variant in both humans and animals. S. Kentucky from humans exhibited high‐level resistance to ciprofloxacin, in addition to a high prevalence of ESBL.

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The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2016

(2017)

Abstract This report of the European Food Safety Authority and the European Centre for Disease Prevention and Control presents the results of the zoonoses monitoring activities carried out in 2016 in 37 European countries (28 Member States (MS) and nine non‐MS). Campylobacteriosis was the most commonly reported zoonosis and the increasing European Union (EU) trend for confirmed human cases since 2008 stabilised during 2012–2016. In food, the occurrence of Campylobacter remained high in broiler meat. The decreasing EU trend for confirmed human salmonellosis cases since 2008 ended during 2012–2016, and the proportion of human Salmonella Enteritidis cases increased. Most MS met their Salmonella reduction targets for poultry, except five MS for laying hens. At primary production level, the EU‐level flock prevalence of target Salmonella serovars in breeding hens, broilers, breeding and fattening turkeys decreased or stabilised compared with previous years but the EU prevalence of S. Enteritidis in laying hens significantly increased. In foodstuffs, the EU‐level Salmonella non‐compliance for minced meat and meat preparations from poultry was low. The number of human listeriosis confirmed cases further increased in 2016, despite the fact that Listeria seldom exceeds the EU food safety limit in ready‐to‐eat foods. The decreasing EU trend for confirmed yersiniosis cases since 2008 stabilised during 2012–2016, and also the number of confirmed Shiga toxin‐producing Escherichia coli (STEC) infections in humans was stable. In total, 4,786 food‐borne outbreaks, including waterborne outbreaks, were reported. Salmonella was the most commonly detected causative agent – with one out of six outbreaks due to S. Enteritidis – followed by other bacteria, bacterial toxins and viruses. Salmonella in eggs continued to represent the highest risk agent/food combination. The report further summarises trends and sources for bovine tuberculosis, brucellosis, trichinellosis, echinococcosis, toxoplasmosis, rabies, Q fever, West Nile fever and tularaemia.

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Contributors

Jens André Hammerl: Role: Academic Editor

Journal

Journal ID (nlm-ta): Microorganisms

Journal ID (iso-abbrev): Microorganisms

Journal ID (publisher-id): microorganisms

Title: Microorganisms

Publisher: MDPI

ISSN (Electronic): 2076-2607

Publication date (Electronic): 17 May 2021

Publication date Collection: May 2021

Volume: 9

Issue: 5

Electronic Location Identifier: 1077

Affiliations

Bacterial Disease Division, Animal and Plant Quarantine Agency, 177 Hyeksin 8-ro, Gimcheon-si 39660, Gyeongsangbuk-do, Korea; wlgus01@ 123456korea.kr (J.-H.C.); ansehdcks@ 123456korea.kr (D.C.M.); abrahamf@ 123456korea.kr (A.F.M.); kanghy7734@ 123456korea.kr (H.Y.K.); kimsujeong27@ 123456gmail.com (S.-J.K.); shj0211@ 123456korea.kr (H.-J.S.); yoonss24@ 123456korea.kr (S.-S.Y.)

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[* ]Correspondence: imsk0049@ 123456korea.kr ; Tel.: +82-54-912-0738

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Dong Chan Moon https://orcid.org/0000-0003-1244-201X

Soon-Seek Yoon https://orcid.org/0000-0003-0908-8785

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Publisher ID: microorganisms-09-01077

DOI: 10.3390/microorganisms9051077

PMC ID: 8156767

PubMed ID: 34067855

SO-VID: b9143cbb-ec68-4b2a-8268-dbd83122834c

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Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( https://creativecommons.org/licenses/by/4.0/).

Antimicrobial Resistance Profiles and Macrolide Resistance Mechanisms of Campylobacter coli Isolated from Pigs and Chickens

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Most cited references 64

Multilocus sequence typing system for Campylobacter jejuni.

The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017

The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2016

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