Development of Macrolide-Resistant Campylobacter in Broilers Administered Subtherapeutic or Therapeutic Concentrations of Tylosin†

The use of antimicrobials in food animal production, particularly those commonly used to treat infections in humans, has become a source of debate in recent years. However, limited data are available regarding the development of resistance following the subtherapeutic or therapeutic administration of antimicrobials in animal production. The objective of this study was to evaluate the effect of the administration of therapeutic and subtherapeutic concentrations of tylosin on the erythromycin susceptibility of Campylobacter jejuni and Campylobacter coli isolated from the ceca of treated broilers. In three replicated studies, day-of-hatch chicks were exposed to macrolide-susceptible C. jejuni or C. coli. At 2 weeks of age, tylosin was administered at subtherapeutic (22 ppm, continuously in the diet) or therapeutic concentrations (529 ppm, in the drinking water for 5 days). Broilers were sacrificed weekly. Total and erythromycin-resistant Campylobacter spp. were enumerated from individual ceca plus cecal contents. Overall erythromycin resistance was observed at a higher frequency (P < 0.01) among C. coli isolates (70.8%) than among C. jejuni isolates (36.8%) following tylosin administration. Across Campylobacter species, erythromycin resistance was observed at a higher frequency (P < 0.001) when tylosin was administered at subtherapeutic (62.7%) than at therapeutic (11.4%) concentrations. Subtherapeutic administration resulted in the recovery of 83.3 and 56.1% erythromycin-resistant isolates compared with only 33.3 and 7.9% of the isolates expressing erythromycin resistance following the administration of therapeutic concentrations for C. coli and C. jejuni, respectively. Further studies are needed to determine the factors involved in the apparent difference in the acquisition of macrolide resistance in C. coli compared with C. jejuni.

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Method-Dependent Variability in Determination of Prevalence of Campylobacter jejuni and Campylobacter coli in Canadian Retail Poultry

Journal of Food Protection ◽

10.4315/0362-028x.jfp-14-133 ◽

2014 ◽

Vol 77 (10) ◽

pp. 1682-1688 ◽

Cited By ~ 9

Author(s):

CATHERINE D. CARRILLO ◽

DANIEL PLANTE ◽

IRÈNE IUGOVAZ ◽

ROBYN KENWELL ◽

GHISLAINE BÉLANGER ◽

...

Keyword(s):

Campylobacter Coli ◽

Testing Methods ◽

Poultry Products ◽

Thermophilic Campylobacter ◽

Microbiological Methods ◽

Bacterial Gastroenteritis ◽

Campylobacter Species ◽

Raw Poultry ◽

Campylobacter Spp

Campylobacter is the most frequent cause of bacterial gastroenteritis in Canada, and the illness is commonly associated with poultry consumption. Whereas Canadian retail poultry is often contaminated with campylobacters, studies on the prevalence of this organism are inconsistent due to variability in sampling and microbiological methodology. To determine the current microbiological status of Canadian poultry, and to evaluate two commonly used microbiological methods, 348 raw poultry samples were collected at retail across Canada over a period of 3 years (2007 to 2010) and were analyzed for the presence of thermophilic Campylobacter species. The overall prevalence of Campylobacter spp. was found to be 42.8% by a combination of the two testing methods, with 33.9% of the samples positive for C. jejuni, 3.7% of the samples positive for C. coli, and 5.2% of the samples positive for both. Variability in Campylobacter spp. prevalence was observed in samples obtained from different regions across Canada and from poultry with or without skin, but this was not statistically significant. In co-contaminated samples, C. jejuni was preferentially recovered from Preston agar compared with mCCDA and Campy-Cefex agar, with an increase in recovery of C. coli on all selective media after 48 h of enrichment. A subset of 214 of the poultry rinses were analyzed by both Health Canada's standard method, MFLP-46 (enrichment in Park and Sanders broth), and a second method requiring enrichment in Bolton broth. Significantly more positive samples were obtained with the MFLP-46 method (40.6%) than with the alternate method (35.0%). This improved recovery with MFLP-46 may be due to the omission of cycloheximide from this method. These results demonstrate that determination of prevalence of Campylobacter spp. on poultry products may be significantly impacted by the choice of microbiological methods used. Canadian poultry continues to be a source of exposure to Campylobacter spp.

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Genetic characterisation of virulence genes associated with adherence, invasion and cytotoxicity in Campylobacter spp. isolated from commercial chickens and human clinical cases

Onderstepoort Journal of Veterinary Research ◽

10.4102/ojvr.v85i1.1507 ◽

2018 ◽

Vol 85 (1) ◽

Cited By ~ 6

Author(s):

Samantha Reddy ◽

Oliver T. Zishiri

Keyword(s):

South Africa ◽

Campylobacter Jejuni ◽

Virulence Genes ◽

Clinical Isolates ◽

Lower Percentage ◽

Campylobacter Coli ◽

Faecal Samples ◽

Commercial Chicken ◽

Campylobacter Species ◽

Campylobacter Spp

Virulence-associated genes have been recognised and detected in Campylobacter species. The majority of them have been proven to be associated with pathogenicity. This study aimed to detect the presence of virulence genes associated with pathogenicity and responsible for invasion, expression of adherence, colonisation and production of the cytolethal distending toxin (cdt) in Campylobacter jejuni and Campylobacter coli. Commercial chicken faecal samples were randomly sampled from chicken farms within the Durban metropolitan area in South Africa. Furthermore, human clinical Campylobacter spp. isolates were randomly sampled from a private pathology laboratory in South Africa. Out of a total of 100 chicken faecal samples, 78% (n = 78) were positive for Campylobacter growth on modified charcoal cefoperazone deoxycholate and from the random laboratory collection of 100 human clinical isolates, 83% (n = 83) demonstrated positive Campylobacter spp. growth following culturing methods. These samples were screened for the presence of the following virulence genes: cadF, hipO, asp, ciaB, dnaJ, pldA, cdtA, cdtB and cdtC. As expected, the cadF gene was present in 100% of poultry (n = 78) and human clinical isolates (n = 83). Campylobacter jejuni was the main species detected in both poultry and human clinical isolates, whilst C. coli were detected at a significantly lower percentage (p < 0.05). Eight per cent of the C. jejuni from human clinical isolates had all virulence genes that were investigated. Only one C. coli isolate demonstrated the presence of all the virulence genes investigated; however, the pldA virulence gene was detected in 100% of the C. coli isolates in poultry and a high percentage (71%) in human clinical C. coli isolates as well. The detection of cdt genes was found at higher frequency in poultry than human clinical isolates. The high prevalence rates of virulence genes detected in poultry and human clinical isolates demonstrate their significance in the pathogenicity of Campylobacter species.

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Prevalence of Campylobacter spp. in Retail Chicken, Turkey, Pork, and Beef Meat in Poland between 2009 and 2013

Journal of Food Protection ◽

10.4315/0362-028x.jfp-14-353 ◽

2015 ◽

Vol 78 (5) ◽

pp. 1024-1028 ◽

Cited By ~ 23

Author(s):

DOROTA KORSAK ◽

ELŻBIETA MAĆKIW ◽

ELŻBIETA ROŻYNEK ◽

MONIKA ŻYŁOWSKA

Keyword(s):

Control Point ◽

Retail Trade ◽

Campylobacter Coli ◽

Turkey Meat ◽

Critical Control Point ◽

Beef Meat ◽

Thermophilic Campylobacter ◽

Campylobacter Species ◽

Meat Samples ◽

Campylobacter Spp

The purpose of the present study was to determine the prevalence of thermophilic Campylobacter in poultry, pork, and beef meat at the retail level and to identify the main categories of meat representing the most significant reservoirs of Campylobacter. A monitoring study was conducted throughout Poland from 2009 to 2013. A total of 1,700 fresh meat samples were collected from supermarkets, large retail outlets, and smaller stores. Thermophilic Campylobacter species were detected in 690 (49.3%) of 1,400 poultry samples collected from retail trade. Strains were isolated from 50.2 and 41.1% of raw chicken and turkey meat samples, respectively, and from 50.1 and 42.6% of raw chicken and turkey giblets. The incidence of Campylobacter spp. on pork (10.6%) and beef (10.1%) was significantly lower than on poultry. Campylobacter jejuni was the most prevalent Campylobacter species in chicken (46.6%), pork (68.6%), and beef (66.7%), and Campylobacter coli was the most frequently isolated Campylobacter species in turkey meat (71.2%). This study revealed that retail raw meats are often contaminated with Campylobacter; however, the prevalence of these pathogens is markedly different in different meats. Raw retail meats are potential vehicles for transmitting foodborne diseases, and our findings stress the need for increased implementation of hazard analysis critical control point programs and consumer food safety education efforts.

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Campylobacter species in animal, food, and environmental sources, and relevant testing programs in Canada

Canadian Journal of Microbiology ◽

10.1139/cjm-2014-0770 ◽

2015 ◽

Vol 61 (10) ◽

pp. 701-721 ◽

Cited By ~ 25

Author(s):

Hongsheng Huang ◽

Brian W. Brooks ◽

Ruff Lowman ◽

Catherine D. Carrillo

Keyword(s):

Meat Products ◽

Raw Milk ◽

Campylobacter Coli ◽

Public Health Burden ◽

Wide Range ◽

Significant Public Health ◽

Campylobacter Species ◽

Campylobacter Lari ◽

Human Infections ◽

Campylobacter Spp

Campylobacter species, particularly thermophilic campylobacters, have emerged as a leading cause of human foodborne gastroenteritis worldwide, with Campylobacter jejuni, Campylobacter coli, and Campylobacter lari responsible for the majority of human infections. Although most cases of campylobacteriosis are self-limiting, campylobacteriosis represents a significant public health burden. Human illness caused by infection with campylobacters has been reported across Canada since the early 1970s. Many studies have shown that dietary sources, including food, particularly raw poultry and other meat products, raw milk, and contaminated water, have contributed to outbreaks of campylobacteriosis in Canada. Campylobacter spp. have also been detected in a wide range of animal and environmental sources, including water, in Canada. The purpose of this article is to review (i) the prevalence of Campylobacter spp. in animals, food, and the environment, and (ii) the relevant testing programs in Canada with a focus on the potential links between campylobacters and human health in Canada.

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Antimicrobial resistance and interspecies gene transfer in Campylobacter coli and Campylobacter jejuni isolated from food animals, poultry processing, and retail meat in North Carolina, 2018–2019

PLoS ONE ◽

10.1371/journal.pone.0246571 ◽

2021 ◽

Vol 16 (2) ◽

pp. e0246571

Author(s):

Dawn M. Hull ◽

Erin Harrell ◽

Arnoud H. M. van Vliet ◽

Maria Correa ◽

Siddhartha Thakur

Keyword(s):

Public Health ◽

North Carolina ◽

Gene Transfer ◽

Antimicrobial Resistance ◽

Virulence Factors ◽

Animal Production ◽

Campylobacter Coli ◽

Food Animal ◽

Retail Meat ◽

Food Animals

The Center for Disease Control and Prevention identifies antimicrobial resistant (AMR) Campylobacter as a serious threat to U.S. public health due to high community burden, increased transmissibility, and limited treatability. The National Antimicrobial Resistance Monitoring System (NARMS) plays an important role in surveillance of AMR bacterial pathogens in humans, food animals and retail meats. This study investigated C. coli and C. jejuni from live food animals, poultry carcasses at production, and retail meat in North Carolina between January 2018-December 2019. Whole genome sequencing and bioinformatics were used for phenotypic and genotypic characterization to compare AMR profiles, virulence factors associated with Guillain-Barré Syndrome (GBS) (neuABC and cst-II or cst-III), and phylogenic linkage between 541 Campylobacter isolates (C. coli n = 343, C. jejuni n = 198). Overall, 90.4% (489/541) Campylobacter isolates tested positive for AMR genes, while 43% (233/541) carried resistance genes for three or more antibiotic classes and were classified molecularly multidrug resistant. AMR gene frequencies were highest against tetracyclines (64.3%), beta-lactams (63.6%), aminoglycosides (38.6%), macrolides (34.8%), quinolones (24.4%), lincosamides (13.5%), and streptothricins (5%). A total of 57.6% (114/198) C. jejuni carried GBS virulence factors, while three C. coli carried the C. jejuni-like lipooligosaccharide locus, neuABC and cst-II. Further evidence of C. coli and C. jejuni interspecies genomic exchange was observed in identical multilocus sequence typing, shared sequence type (ST) 7818 clonal complex 828, and identical species-indicator genes mapA, ceuE, and hipO. There was a significant increase in novel STs from 2018 to 2019 (2 in 2018 and 21 in 2019, p<0.002), illustrating variable Campylobacter genomes within food animal production. Introgression between C. coli and C. jejuni may aid pathogen adaption, lead to higher AMR and increase Campylobacter persistence in food processing. Future studies should further characterize interspecies gene transfer and evolutionary trends in food animal production to track evolving risks to public health.

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Antimicrobial resistance among Campylobacter spp. strains isolated from faecal samples of pigs chickens and ducks at Dong Thap province

Science and Technology Development Journal ◽

10.32508/stdj.v19i1.543 ◽

2016 ◽

Vol 19 (1) ◽

pp. 45-54

Author(s):

Thuy Thu Cao ◽

Hoang Van Minh Nguyen ◽

Hien Tinh Tran ◽

James Ian Campbell ◽

Stephen Baker ◽

...

Keyword(s):

23S Rrna ◽

Rrna Gene ◽

Campylobacter Coli ◽

Erythromycin Resistance ◽

Gyra Gene ◽

Pump System ◽

Double Mutation ◽

Faecal Samples ◽

23S Rrna Gene ◽

Campylobacter Spp

This study was designed to identify the genetic basis that results in the development of antibiotic resistance in Campylobacter spp. We carried out a molecular examination of 75 strains looking for resistance factors. These strains were isolated from faecal samples of pigs, chickens and ducks at Dong Thap province. There were 89.3 % strains which showed mutations on DNA gyrase-gyrA gene at the position 86 (C257T and T227G). There were also a further 32 % strains that showed mutations on gene cmeR encoding the efflux CmeABC pump system. This study has also shown that 29.3 % of Campylobacter spp. have mutations in fluoroquinolone (FQ) resistance on both genes gyrA and cmeR. In comparison with Campylobacter jejuni with the mutation C257T (Thr-86-Ile), Campylobacter coli has another mutation at T227G (Thr-86-Met). This mutation, encoding FQ resistance, is common in both swine and poultry but has not yet been identified in Viet Nam. As well as FQ resistance, resistance to erythromycine (Ery) has been detected in C. coli, in 10 strains erythromycin resistance, with a mutation at position A2075G. There was 1 strain which carried two mutations A2075G and A2074C at 23S-rRNA gene, and 2 mutant strains with a double mutation at A2075G and A2076C. In summary, there were three strains of C. coli with double mutations encoding Ery resistance at Dong Thap and this resistance characteristic has not been identified eslewhere.

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Prevalence of Thermophilic Campylobacter spp. in Ready-to-Eat Foods and Raw Poultry in Northern Ireland

Journal of Food Protection ◽

10.4315/0362-028x-65.8.1326 ◽

2002 ◽

Vol 65 (8) ◽

pp. 1326-1328 ◽

Cited By ~ 35

Author(s):

JOHN E. MOORE ◽

TOM S. WILSON ◽

DAVID R. A. WAREING ◽

TOM J. HUMPHREY ◽

PHILIP G. MURPHY

Keyword(s):

Northern Ireland ◽

Hazard Analysis ◽

Control Point ◽

Campylobacter Coli ◽

Limited Data ◽

Critical Control Point ◽

Thermophilic Campylobacter ◽

Campylobacter Lari ◽

Raw Poultry ◽

Campylobacter Spp

Although there have been numerous studies investigating the prevalence of campylobacters in animals and raw meats, there are limited data on the persistence of these organisms in ready-to-eat (RTE) foodstuffs. Although poultry is now well established as a major reservoir of thermophilic campylobacters, it is widely assumed that hazard analysis critical control point (HACCP) controls in commercial and industrial settings are effective in eliminating this hazard through thorough cooking of RTE products. Therefore, it was the primary aim of this study to investigate the effectiveness of HACCP controls in eliminating campylobacters in such cooked RTE foods by attempting to isolate viable organisms from product. Concurrently, the results of this study demonstrate that local poultry is highly contaminated with campylobacters. Commercially available RTE foodstuffs (n = 2,030) consisting of 1,061 poultry-related cooked products and 969 other products were analyzed and were not found to contain thermophilic Campylobacter spp. In addition, 107 raw chickens (63 fresh birds and 44 frozen birds) were sampled, and 94% of the fresh birds and 77% of the frozen birds examined were demonstrated to be contaminated with campylobacters, with Campylobacter jejuni, Campylobacter coli, and Campylobacter lari accounting for 69, 30, and 1% of the contaminating organisms, respectively. In general, commercially available RTE foodstuffs, including cooked poultry, are not commonly contaminated with campylobacters and thus do not appear to represent a significant cause of clinical infection of Campylobacter spp. in Northern Ireland. However, raw poultry produce, including fresh and frozen chicken, frequently tested positive for campylobacters. Implementation of HACCP systems by food processors will help to minimize and/or eliminate the risk posed by this organism to the consumer.

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Optimization of the In Vitro Bactericidal Effect of a Mixture of Chlorine and Sodium Gallate against Campylobacter spp. and Arcobacter butzleri

Journal of Food Protection ◽

10.4315/jfp-20-181 ◽

2021 ◽

Vol 84 (7) ◽

pp. 1127-1135

Author(s):

LUIS ENRIQUE ORTIZ-SUÁREZ ◽

MAURICIO REDONDO-SOLANO ◽

MARÍA LAURA ARIAS-ECHANDI ◽

CAROL VALENZUELA-MARTÍNEZ ◽

ETNA AIDA PEÑA-RAMOS

Keyword(s):

Foodborne Pathogens ◽

Bactericidal Effect ◽

Campylobacter Coli ◽

Bactericidal Properties ◽

Bactericidal Effects ◽

Arcobacter Butzleri ◽

Central Composite Experimental Design ◽

Campylobacter Species ◽

Campylobacter Spp

ABSTRACT Campylobacter spp. and Arcobacter butzleri are foodborne pathogens associated with the consumption of contaminated raw chicken meat. At the industry level, the combination of new and common antimicrobials could be used as a strategy to control the presence of pathogens in chicken carcasses. The objective of this study was to determine the bacteriostatic and bactericidal effects of a mixture of chlorine (Cl) and sodium gallate (SG) on a mixture of two Campylobacter species (Campylobacter jejuni and Campylobacter coli) and A. butzleri. Using a central composite experimental design, it was established that the optimum inhibitory SG-Cl concentration for Campylobacter spp. was 44 to 45 ppm. After 15 h of incubation, Campylobacter species growth was reduced by 37.5% and the effect of Cl was potentiated by SG at concentrations above 45 ppm. In the case of A. butzleri, optimum levels of 28 and 41 ppm were observed for SG and Cl, respectively; no synergism was reported, as this bacterium was more sensitive to lower Cl concentrations than Campylobacter. After a 20-min pretreatment with peracetic acid (50 ppm), the optimum condition to achieve a >1.0-Log CFU/mL reduction of Campylobacter spp. was exposure to 177 ppm of Cl and 44 ppm of SG for 56 min. As A. butzleri showed lower resistance to the bacteriostatic effect of the Cl-SG combination, it was assumed that optimum bactericidal conditions for Campylobacter spp. were effective to control the former; this was confirmed with subsequent validation of the model. The SG-Cl combination has bactericidal properties against Campylobacter and A. butzleri, and it may be a useful strategy to improve sanitary practices applied in the poultry industry. HIGHLIGHTS

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Temporal Prevalence of Antimicrobial Resistance in Campylobacter spp. from Beef Cattle in Alberta Feedlots

Applied and Environmental Microbiology ◽

10.1128/aem.02830-05 ◽

2006 ◽

Vol 72 (6) ◽

pp. 4088-4095 ◽

Cited By ~ 27

Author(s):

G. D. Inglis ◽

D. W. Morck ◽

T. A. McAllister ◽

T. Entz ◽

M. E. Olson ◽

...

Keyword(s):

Antimicrobial Resistance ◽

Beef Cattle ◽

Antimicrobial Agents ◽

Multidrug Resistant ◽

Campylobacter Coli ◽

Erythromycin Resistance ◽

Fecal Samples ◽

Minimal Impact ◽

Long Acting ◽

Campylobacter Spp

ABSTRACT Antimicrobial resistance (AMR) was temporally assessed in campylobacters isolated from beef cattle (7,738 fecal samples from 2,622 animals) in four commercial feedlots in Alberta. All calves were administered chlortetracycline and oxytetracycline in feed, and a majority of the animals (93%) were injected with long-acting oxytetracycline upon arrival at the feedlot. Fecal samples from individual animals were collected upon arrival (i.e., entry sample), 69 days (standard deviation [SD] = 3 days) after arrival (i.e., interim sample), and 189 days (SD = 33 days) after arrival (i.e., exit sample) at the feedlot. In total, 1,586 Campylobacter isolates consisting of Campylobacter coli (n = 154), Campylobacter fetus (n = 994), Campylobacter jejuni (n = 431), Campylobacter hyointestinalis (n = 4), and Campylobacter lanienae (n = 3) were recovered and characterized. The administration of antimicrobials did not decrease carriage rates of campylobacters, and minimal resistance (≤4%) to azithromycin, ciprofloxacin, enrofloxacin, gentamicin, and meropenem was observed. In contrast, substantive increases in the prevalence of isolates resistant to tetracycline and doxycycline (56 to 89%) for C. coli, C. fetus, and C. jejuni, as well as in the number of animals (7 to 42%) from which resistant isolates were recovered, were observed during the feedlot period. Increased resistance to erythromycin (total isolates and carriages rates) was also observed in isolates of C. coli over the three isolation times. The majority of C. fetus isolates recovered were resistant to nalidixic acid, but this was independent of when they were isolated. A relatively limited number of multidrug-resistant isolates were recovered and consisted primarily of C. coli resistant to tetracyclines and erythromycin (10% of isolates). Over the course of the feedlot period, considerable increases in antimicrobial resistance were observed in C. coli, C. fetus, and C. jejuni, but with the exception of erythromycin resistance in C. coli, the administration of antimicrobial agents to beef cattle was found to have a minimal impact on resistance to macrolides and fluoroquinolones, the two classes of antimicrobials used to treat campylobacteriosis in humans. However, the widespread use of antimicrobial agents in beef production and the possible horizontal transfer of mobile genetic elements with antimicrobial resistance determinants among Campylobacter and other bacterial taxa emphasize the need to monitor AMR development in bacteria from beef cattle.

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

Microorganisms ◽

10.3390/microorganisms9051077 ◽

2021 ◽

Vol 9 (5) ◽

pp. 1077

Author(s):

Ji-Hyun Choi ◽

Dong Chan Moon ◽

Abraham Fikru Mechesso ◽

Hee Young Kang ◽

Su-Jeong Kim ◽

...

Keyword(s):

Nalidixic Acid ◽

Ribosomal Proteins ◽

Resistance Mechanisms ◽

23S Rrna ◽

Considerable Proportion ◽

Rrna Gene ◽

Campylobacter Coli ◽

Erythromycin Resistance ◽

Public Health Hazards ◽

Resistance Rates

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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