Decreased Resistance to Broad-Spectrum Cephalosporin in <i>Escherichia coli</i> from Healthy Broilers at Farms in Japan After Voluntary Withdrawal of Ceftiofur

Hiki, Mototaka; Kawanishi, Michihiro; Abo, Hitoshi; Kojima, Akira; Koike, Ryuji; Hamamoto, Shuichi; Asai, Tetsuo

doi:10.1089/fpd.2015.1960

Cited by 55 publications

(40 citation statements)

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“…Examination of the indicator E. coli in our study clearly demonstrates a decrease in prevalence of samples harboring isolates positive for the ESBL/AmpC resistance genes bla CMY-2 and bla CTX-M in the meconium of newly hatched birds after the cessation of in ovo administration of ceftiofur. This finding shows a beneficial effect of the cessation of the use of ceftiofur, reinforcing the findings of other studies where a decrease in resistance to extended spectrum cephalosporins was observed (4, 9, 12). Nevertheless, we did not observe an effect in the broilers, as was the case in the previous studies (7).…”

Section: Discussionsupporting

confidence: 90%

“…One of the most important causes of early mortality in broiler chick is omphalitis, mostly caused by avian pathogenic E. coli (APEC), a subgroup of extra-intestinal pathogenic E. coli (ExPEC) (1, 2). Ceftiofur, a third generation cephalosporin antimicrobial, has been administered for over 15 years either in ovo or by subcutaneous injection at the hatchery, in order to reduce early chick mortality in many countries (3) Consequently, an increased prevalence of extended-spectrum β-lactamase (ESBL) and AmpC β-lactamase producing Escherichia coli has been reported worldwide (4-7), resulting in an increased extended spectrum cephalosporin resistance in the broiler poultry chain production. This is a public health concern due to co-resistance with other extended spectrum cephalosporins, such as ceftriaxone and cephamycin, antimicrobials which are used widely in human medicine (8, 9).…”

Section: Introductionmentioning

confidence: 99%

“…Recent studies have shown a decrease in the proportion of clinical isolates possessing ESBL/AmpC-associated resistance genes after this second cessation (6, 12, 13). In addition, the prevalence of resistant E. coli from healthy broilers at farms was markedly decreased within a year after ceftiofur cessation at hatcheries in Japan (4). A decrease in the prevalence of Salmonella harboring bla CMY-2 in chicken meat was also observed in Japan in the same years (14).…”

Section: Introductionmentioning

confidence: 99%

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Effect of ceftiofur cessation and substitution with lincomycin-spectinomycin on extended-spectrum-beta-lactamase/AmpC genes and multidrug resistance in E. coli from a Canadian broiler production pyramid

Verrette¹,

Fairbrother

Boulianne

2019

Preprint

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24Ceftiofur, a cephalosporin antimicrobial, was used systematically in Canadian hatcheries 25 for many years to prevent early mortality in chicks leading to a high prevalence of 26 cephalosporin resistance in Escherichia coli in chickens. Preventive use of ceftiofur in 27 hatcheries ceased in 2014. We examined the effect of ceftiofur cessation and replacement 28 with lincomycin-spectinomycin at the hatchery on the proportion of E. coli positive for 29 extended-spectrum β-lactamase (ESBL) and AmpC β-lactamase related genes, and on the 30resistance profiles of ESBL/AmpC positive E. coli in broilers and their 31 associated breeders, at one year post-cessation. For indicator E. coli from non-enriched 32 media, a significant decrease post-cessation in the proportion of samples harboring E. coli 33 isolates positive for bla CMY-2 and/or bla CTX-M was observed. In contrast, following 34 enrichment in medium containing ceftriaxone (1mg/L) to facilitate recovery of 35 ESBL/AmpC β-lactamase producing E. coli colonies, both pre-and post-cessation, 99% 36 of the samples harbored E. coli positive for bla CMY-2 or bla CTX-M . Flocks receiving 37lincomycin-spectinomycin after cessation of ceftiofur showed a significantly greater non-38 susceptibility to aminoglycoside, folate inhibitor, phenicol, tetracycline and possible 39 extensively drug resistant E. coli compared to those receiving ceftiofur or no 40 antimicrobial at hatchery. This study clearly demonstrates an initial decrease in 41 ESBL/AmpC positive E. coli following the cessation of ceftiofur in hatchery but an 42 increase in multidrug resistant E. coli following replacement with lincomycin-43 spectinomycin. 44 Importance 45Antimicrobial resistance is a global problem. The antimicrobial ceftiofur has been used 46 worldwide for disease prevention in poultry production resulting in a greatly increased 47 resistance to this antimicrobial important in poultry and human medicine. Our study 48 examines the impact of ceftiofur cessation and its replacement with the antimicrobial 49 combination lincomycin-spectinomycin, a common practice in the industry. Our study 50 demonstrated a decrease in ceftiofur resistance after the cessation of its use, although the 51 resistance genes remain ubiquitous in all phases of poultry production, showing that 52 poultry remains a reservoir for ceftiofur resistance and requiring continued vigilance. We 53 also observed a decrease in multidrug resistance after cessation of ceftiofur although the 54 contrary finding following use of lincomycin-spectinomycin indicates that the use of 55 these antimicrobials should be questioned. Reduced resistance to ceftiofur in poultry may 56 translate to better treatment efficacy, decreased morbidity, mortality, duration and cost of 57 hospitalization in humans. 58 Introduction 59One of the most important causes of early mortality in broiler chick is omphalitis, mostly 60 caused by avian pathogenic E. coli (APEC), a subgroup of extra-intestinal pathogenic E. 61 coli (ExPEC) (1, 2). Ceftiofur, a third generati...

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Section: Discussionsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Effect of ceftiofur cessation and substitution with lincomycin-spectinomycin on extended-spectrum-beta-lactamase/AmpC genes and multidrug resistance in E. coli from a Canadian broiler production pyramid

Verrette¹,

Fairbrother

Boulianne

2019

Preprint

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“…Recent Canadian studies have shown a decrease in the proportion of clinical isolates possessing ESBL/AmpC-associated resistance genes after the second cessation in 2014 (13)(14)(15). In addition, the prevalence of resistant E. coli from healthy broilers on farms was decreased within a year after ceftiofur cessation at hatcheries in Japan, from 16.4% in 2010 and 16.8% in 2011 to 9.2% in 2012 and 4.6% in 2013 (4). A decrease in the prevalence of Salmonella harboring bla CMY-2 in chicken meat was also observed in Japan in the same years (16).…”

mentioning

confidence: 84%

“…Ceftiofur, a third-generation cephalosporin antimicrobial, has been administered for over 15 years either in ovo or by subcutaneous injection at the hatchery, in order to reduce early chick mortality in many countries (3). Consequently, an increased prevalence of extended-spectrum-␤-lactamase (ESBL) and AmpC ␤-lactamase-producing Escherichia coli has been reported worldwide (4)(5)(6); this increased prevalence has resulted in an increased resistance to extended-spectrum cephalosporins in the broiler poultry production chain. This is a public health concern due to cross-resistance with other extended-spectrum cephalosporins, such as ceftriaxone and cephamycin, antimicrobials that are used widely in human medicine and classified by the World Health Organization as highest-priority critically important antimicrobials (7)(8)(9)(10).…”

mentioning

confidence: 99%

Effect of Cessation of Ceftiofur and Substitution with Lincomycin-Spectinomycin on Extended-Spectrum-β-Lactamase/AmpC Genes and Multidrug Resistance in Escherichia coli from a Canadian Broiler Production Pyramid

Verrette

Fairbrother

Boulianne

2019

Appl Environ Microbiol

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Ceftiofur, a third-generation cephalosporin antimicrobial, was used in Canadian hatcheries for many years to prevent early mortality in chicks, leading to a high prevalence of cephalosporin resistance in Escherichia coli in chickens. Preventive use of ceftiofur in hatcheries ceased in 2014. We examined the effect of ceftiofur cessation (n ϭ 40 flocks with ceftiofur and n ϭ 28 flocks without antimicrobial at hatchery) and its replacement with an antimicrobial combination, lincomycinspectinomycin (n ϭ 32), at the hatchery on the proportion of samples with E. coli positive for extended-spectrum-␤-lactamase (ESBL) and AmpC ␤-lactamase-related genes, and on the multidrug resistance profiles of ESBL/AmpC-positive E. coli in broilers and their associated breeders (n ϭ 46 samples), at 1 year postcessation. For indicator E. coli from nonenriched media, a significant decrease postcessation in the proportion of samples harboring E. coli isolates positive for bla CMY-2 and/or bla CTX-M was observed. In contrast, following enrichment in medium containing ceftriaxone (1 mg/liter) to facilitate recovery of ESBL/AmpC ␤-lactamase-producing E. coli colonies, both pre-and postcessation, 99% of the samples harbored E. coli positive for bla CMY-2 or bla CTX-M . Among the 15 tested antimicrobial agents, flocks receiving lincomycin-spectinomycin after cessation of ceftiofur showed a significantly greater nonsusceptibility to aminoglycosides, folate inhibitors, phenicols, and tetracyclines and a greater proportion of possible extensively drug-resistant E. coli than those receiving ceftiofur or no antimicrobial at hatchery. This study clearly demonstrates an initial decrease in ESBL/AmpC-positive E. coli following the cessation of ceftiofur in the hatchery but an increase in antimicrobial non-␤-lactam resistance of ESBL/ AmpC-positive E. coli following replacement with lincomycin-spectinomycin. IMPORTANCE Antimicrobial resistance is a global problem. The antimicrobial ceftiofur has been used worldwide for disease prevention in poultry production, resulting in a greatly increased resistance to this antimicrobial important in poultry and human medicine. Our study examined the impact of ceftiofur cessation and its replacement with the antimicrobial combination lincomycin-spectinomycin, a common practice in the industry. Our study demonstrated a decrease in ceftiofur resistance after the cessation of ceftiofur use, although the resistance genes remain ubiquitous in all phases of poultry production, showing that poultry remains a reservoir for ceftiofur resistance and requiring continued vigilance. We also observed a decrease in multidrug resistance involving different antimicrobial classes after cessation of ceftiofur but an increase following use of lincomycin-spectinomycin, indicating that this antimicrobial use should be questioned. Reduced resistance to ceftiofur in poultry may translate to better treatment efficacy, decreased morbidity/mortality, and enhanced food safety for humans.Citation Verrette L, Fairbrother JM, Boulianne M. 2019....

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Antimicrobial Resistance Paradigm and One-Health Approach

Singh

Anand²,

Dholpuria

et al. 2020

Sustainable Agriculture Reviews

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Decreased Resistance to Broad-Spectrum Cephalosporin in Escherichia coli from Healthy Broilers at Farms in Japan After Voluntary Withdrawal of Ceftiofur

Cited by 55 publications

References 10 publications

Effect of ceftiofur cessation and substitution with lincomycin-spectinomycin on extended-spectrum-beta-lactamase/AmpC genes and multidrug resistance in E. coli from a Canadian broiler production pyramid

Effect of ceftiofur cessation and substitution with lincomycin-spectinomycin on extended-spectrum-beta-lactamase/AmpC genes and multidrug resistance in E. coli from a Canadian broiler production pyramid

Effect of Cessation of Ceftiofur and Substitution with Lincomycin-Spectinomycin on Extended-Spectrum-β-Lactamase/AmpC Genes and Multidrug Resistance in Escherichia coli from a Canadian Broiler Production Pyramid

Antimicrobial Resistance Paradigm and One-Health Approach

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