The dynamics of the antibiotic resistome in the feces of freshly weaned pigs following therapeutic administration of oxytetracycline

Ghanbari, Mahdi; Klose, Viviana; Crispie, Fiona; Cotter, Paul D.

doi:10.1038/s41598-019-40496-8

Cited by 48 publications

(75 citation statements)

References 53 publications

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“…ing revealed a diverse set of AMR genes in the presence and absence of antimicrobial treatment, which reflects findings in other recent work 19 . Specifically, genes associated with tetracycline and macrolide resistance predominated.…”

Section: High Amr Gene Diversity and Cross-class Resistance Genes In supporting

confidence: 89%

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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Section: High Amr Gene Diversity and Cross-class Resistance Genes In supporting

confidence: 89%

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

Pollock

Muwonge

Hutchings

et al. 2020

Sci Rep

View full text Add to dashboard Cite

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“…The shotgun metagenomics revealed a diverse set of AMR genes in the presence and absence of antimicrobial treatment, which reflects findings in other recent work (26). Specifically, genes associated with tetracycline and macrolide resistance predominated.…”

Section: Discussionsupporting

confidence: 86%

“…Metagenomic data has revealed associations between antibiotic usage in pigs and poultry with increases in AMR gene prevalence, with lower AMR gene diversity, but higher AMR gene loads being observed on pig units in comparison to poultry units (25). Administration of oxytetracycline immediately post-weaning has also been shown to increase the abundance of AMR genes conferring tetracycline, beta-lactam and multi-drug resistance (26). The persistence of AMR genes on pig units has also been assessed, with differences in specific AMR gene levels being observed when comparing samples from sows and finishers (27).…”

Section: Introductionmentioning

confidence: 99%

Resistance to change? The impact of group medication on AMR gene dynamics during commercial pig production

Pollock

Muwonge

Hutchings

et al. 2019

Preprint

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The anthropogenic selection of antimicrobial resistance (AMR) genes is under intense scrutiny, particularly in livestock production, where group antimicrobial administration is used to control disease. Whilst large epidemiological studies provide important data on the diversity and distribution of AMR genes, we have little insight into how group antimicrobial administration impacts AMR gene abundance and diversity within a system. Here, faecal microbiome and AMR gene dynamics were tracked for six months through a standard production cycle on a commercial pig unit. Our results demonstrate that specific AMR genes have reached an equilibrium across this farming system to the extent that the levels measured were maintained from suckling through to slaughter, despite increases in microbiome diversity in early development. These levels were not influenced by antibiotic use, either during the production cycle or following whole herd medication. Some AMR genes were found at levels higher than that of the bacterial 16S rRNA gene, indicating widespread distribution across the most common bacterial genera. The targeted AMR genes were also detected in nearby soil samples, several with decreasing abundance with increasing distance from the unit, demonstrating that the farm acts as a point source of AMR gene ‘pollution’. Metagenomic sequencing of a subset of samples identified 144 AMR genes, with higher gene diversity in the piglet samples compared to the sow samples. Critically, despite overwhelming and stable levels of resistance alleles against the main antimicrobials used on this farm, these compounds continue to control the bacterial pathogens responsible for production losses and compromised welfare.ImportanceGroup antibiotic treatment has been used for decades to control bacterial diseases that reduce the productivity and compromise the welfare of livestock. Recent increases in antibiotic resistant infections in humans has resulted in concerns that antibiotic use in livestock may contribute to the development of untreatable bacterial infections in humans. There is however little understanding as to how the genes that bacteria require to become resistant to antibiotics respond during and after group antibiotic treatment of livestock, particularly in systems where high levels of antibiotics have been used for a prolonged period of time. We show that in such a system, levels of specific antibiotic resistance genes are high irrespective of group antibiotic treatments, whilst dramatic reductions in antibiotic use also fail to reduce the levels of these genes. These findings have important implications for public policy relating to the use of antibiotic in livestock farming.

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“…The swine gastrointestinal microbiota harbors a diverse population of bacteria that play a role in pig health (2)(3)(4) but may also be a source of antibiotic resistance genes (ARG) (5). Disturbances to the gut microbiota may enhance ARG transfer and/or enhance abundance of antibiotic resistant bacteria shed from the animal (6,7). Post-weaning piglets are highly susceptible to a number of diseases, and prophylactic oral antibiotics (in-feed or in-water) are commonly administered to prevent disease (8,9).…”

Section: Introductionmentioning

confidence: 99%

Toward Antibiotic Stewardship: Route of Antibiotic Administration Impacts the Microbiota and Resistance Gene Diversity in Swine Feces

et al. 2020

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The dynamics of the antibiotic resistome in the feces of freshly weaned pigs following therapeutic administration of oxytetracycline

Cited by 48 publications

References 53 publications

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

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

Resistance to change? The impact of group medication on AMR gene dynamics during commercial pig production

Toward Antibiotic Stewardship: Route of Antibiotic Administration Impacts the Microbiota and Resistance Gene Diversity in Swine Feces

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