Association between selected antimicrobial resistance genes and antimicrobial exposure in Danish pig farms

Birkegård, Anna Camilla; Halasa, Tariq Hisham Beshara; Græsbøll, Kaare; Clasen, Julie; Folkesson, Anders; Toft, Nils

doi:10.1038/s41598-017-10092-9

Cited by 35 publications

(19 citation statements)

References 41 publications

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“…The majority of the studies modelled phenotypic AMR, while few models represented genotypic AMR (Table 5 ). Modelling genotypic AMR can be more complicated as many genes can be linked to a specific antibiotic, and the relationship between gene abundance and antibiotic use seems to be more complex than first anticipated [ 65 ]. Modelling genotypic AMR requires the relevant genes for the modelled AMR to be represented, as well as circumstances allowing for the genetic AMR to be expressed as phenotypic AMR, leading to a spread of the resistant pathogen within the population.…”

Section: Discussionmentioning

confidence: 99%

Send more data: a systematic review of mathematical models of antimicrobial resistance

Birkegård

Halasa

Toft

et al. 2018

Antimicrob Resist Infect Control

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BackgroundAntimicrobial resistance is a global health problem that demands all possible means to control it. Mathematical modelling is a valuable tool for understanding the mechanisms of AMR development and spread, and can help us to investigate and propose novel control strategies. However, it is of vital importance that mathematical models have a broad utility, which can be assured if good modelling practice is followed.ObjectiveThe objective of this study was to provide a comprehensive systematic review of published models of AMR development and spread. Furthermore, the study aimed to identify gaps in the knowledge required to develop useful models.MethodsThe review comprised a comprehensive literature search with 38 selected studies. Information was extracted from the selected papers using an adaptation of previously published frameworks, and was evaluated using the TRACE good modelling practice guidelines.ResultsNone of the selected papers fulfilled the TRACE guidelines. We recommend that future mathematical models should: a) model the biological processes mechanistically, b) incorporate uncertainty and variability in the system using stochastic modelling, c) include a sensitivity analysis and model external and internal validation.ConclusionMany mathematical models of AMR development and spread exist. There is still a lack of knowledge about antimicrobial resistance, which restricts the development of useful mathematical models.

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Section: Discussionmentioning

confidence: 99%

Send more data: a systematic review of mathematical models of antimicrobial resistance

Birkegård

Halasa

Toft

et al. 2018

Antimicrob Resist Infect Control

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“…In fact, the largest increases in AMR gene abundance were seen across all genes and in both classes of stock at the same time (W21-W24) which coincided with an increase in 16S rRNA gene copies, hence suggesting an as yet undefined environmental influence on bacterial load and consequently AMR gene abundance. A previous cross-sectional study highlighted that only 10-42% of the variation in AMR gene levels could be explained by factors included in statistical models (including lifetime antimicrobial exposure), suggesting that AMR gene levels are strongly influenced by a variety of other elements 43 . Whilst these could be related to feed changes, the fact that the dry sows and young pigs were housed differently and fed different diets 44 would suggest that this effect is due to some other factors affecting the entire farm, such as housing and management 35,45,46 , environmental conditions 46 or the introduction of an infectious agent.…”

Section: Changes In Amr Gene Abundances Were Not Associated With Antimentioning

confidence: 99%

Resistance to change: AMR gene dynamics on a commercial pig farm with high antimicrobial usage

Pollock

Muwonge

Hutchings

et al. 2020

Sci Rep

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Group antimicrobial administration is used to control disease in livestock, but we have little insight into how this impacts antimicrobial resistance (AMR) gene dynamics. Here, a longitudinal study was carried out during a single production cycle on a commercial pig unit with high historic and current antimicrobial usage. Quantitative PCR, 16S rRNA gene metabarcoding and shotgun metagenomic sequencing were used to track faecal AMR gene abundance and diversity and microbiome alpha diversity. Shotgun metagenomic sequencing identified 144 AMR genes in total, with higher AMR gene diversity present in young pigs compared to dry sows. Irrespective of in-feed antibiotic treatment or changes in microbiome diversity, mean AMR gene copy number was consistently high, with some AMR genes present at copy numbers comparable to the bacterial 16S rRNA gene. In conclusion, AMR gene prevalence and abundance were not influenced by antibiotic use, either during the production cycle or following whole-herd medication. The high levels of certain genes indicate they are widely disseminated throughout the microbial population, potentially aiding stability. Despite the high and relatively stable levels of resistance genes against the main antimicrobials used, these compounds continue to control production limiting diseases on this unit.Antimicrobial agents are used regularly in many agricultural systems worldwide to improve the health, welfare and productivity of livestock 1,2 . This has led to concerns about the anthropogenic selection of antimicrobial-resistant bacteria in livestock systems 2-4 , particularly due to the potential transfer of antimicrobial resistance (AMR) genes from livestock to humans 5-7 and into the environment 8,9 . In the United Kingdom, 52% of all antimicrobials sold for livestock were used in the pig and poultry sectors, with tetracyclines being reported as the highest sold antibiotic class 10 . Given the substantial use of antimicrobials in pig production, the association between antimicrobial use and AMR has been an area of intensive study. Specifically, antimicrobial administration has been associated with increased AMR in sentinel bacteria such as Escherichia coli [11][12][13] , Staphylococcus aureus 14,15 , and Campylobacter 16 , Salmonella 17 and Enterococcus 18 species. Molecular studies have revealed a higher richness and diversity of AMR genes in pigs administered oxytetracycline in-feed 19 , with farm origin being associated with AMR gene abundances in faeces at slaughter using both quantitative PCR 20 and metagenomic 21 datasets. However, there are currently few longitudinal studies of AMR in livestock systems, specifically for pig production 22 , with information on antimicrobial use in these systems often derived from national figures, rather than from farm medicines records 12,21 .Here, we examine microbial population dynamics and both AMR gene abundance and diversity on a single pig farm during a six-month production cycle. Faecal samples were collected weekly from a batch of young pigs that were ...

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“…Maintenance of the high proportion of positive samples in the Canadian broilers at 1 year after the cessation of administration of ceftiofur could be explained by environmental contamination which may have persisted after birds ceased to excrete E. coli positive for ESBL/AmpC resistance genes (24). Antimicrobial use causing coselection to other antimicrobial classes, such as penicillin and amoxicillin in the breeder, could also be an important factor (30). For example, Danish broiler flocks which did not receive ceftiofur in ovo (whereas their breeders received it) had significantly higher occurrences of bla CMY-2 when aminopenicillins were used up to 6 months before sampling (23).…”

Section: Discussionmentioning

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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Association between selected antimicrobial resistance genes and antimicrobial exposure in Danish pig farms

Cited by 35 publications

References 41 publications

Send more data: a systematic review of mathematical models of antimicrobial resistance

Send more data: a systematic review of mathematical models of antimicrobial resistance

Resistance to change: AMR gene dynamics on a commercial pig farm with high antimicrobial usage

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

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