The antimicrobial resistance crisis: management through gene monitoring

Michael, Carolyn A.; Franks, Ashley E.; Labbate, Maurizio

doi:10.1098/rsob.160236

Cited by 7 publications

(4 citation statements)

References 49 publications

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“…In agreement with Young pig accommodation Sow barn www.nature.com/scientificreports www.nature.com/scientificreports/ previous work, we showed high levels of all studied AMR genes in the non-medicated dry sows, presumably as a consequence of the strong selection pressure exerted by this farm's history of high antimicrobial usage. The levels of the five AMR genes studied in the young pigs reflected those of the sow population, whilst prolonged exposure to two different in-feed antibiotic regimens in the young pigs and a combined in-feed antibiotic regimen in the dry sows had no marked effect on AMR gene counts, potentially suggesting that they have reached saturation within the faecal bacterial populations 39 . Curiously, the antibiotics used (chlortetracycline and tylosin) were still clinically effective on this farm, suggesting that despite a high abundance of resistance genes within the faecal microbiome, that they were not present, or at least not active, within the organisms of clinical interest, i.e.…”

Section: Measured Amr Genes Consistently High Across the Unit Althoumentioning

confidence: 93%

“…high baseline levels of specific AMR genes 36 and phenotypic resistance in Escherichia coli isolates 37,38 in unmedicated pigs, our initial expectation was that AMR gene abundances would markedly increase in response to antimicrobial administration as a result of selective pressure being exerted on specific genes 39 . In agreement with Young pig accommodation Sow barn www.nature.com/scientificreports www.nature.com/scientificreports/ previous work, we showed high levels of all studied AMR genes in the non-medicated dry sows, presumably as a consequence of the strong selection pressure exerted by this farm's history of high antimicrobial usage.…”

Section: Measured Amr Genes Consistently High Across the Unit Althoumentioning

confidence: 99%

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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: Measured Amr Genes Consistently High Across the Unit Althoumentioning

confidence: 93%

Section: Measured Amr Genes Consistently High Across the Unit Althoumentioning

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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“…In addition, the development of drug-resistant pathogens appeared quickly, while the emergence of multi-drug resistant strains has increased exponentially during the recent years [6].…”

Section: Introductionmentioning

confidence: 99%

Antibacterial Efficacy of Commercially Available Essential Oils Tested Against Drug-Resistant Gram-Positive Pathogens

et al. 2018

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The potential antibacterial activity of basil (Ocimum basilicum), chamomile (Matricaria chamomilla), origanum (Thymus capitatus), tea tree (Melaleuca alternifolia) and thyme (Thymus vulgaris) essential oils, was investigated against 29 Gram-positive bacterial strains isolated from wastewater treatment plants, clinical samples (n = 25) and American Type Culture Collection (ATCC) reference strains (n = 4). Wild bacterial strains included methicillin-resistant Staphylococcus aureus (n = 16) and vancomycin-resistant Enterococcus spp. (n = 9). The antimicrobial activity of the selected oils was studied using the broth macrodilution method. The Minimal Inhibitory Concentration (MIC) values for S. aureus ranged from 0.06 to 0.5% (v/v) for origanum oil, 0.06 to 1% (v/v) for thyme oil, 0.12 to 1% (v/v) for tea tree oil, 0.25 to 4% (v/v) for basil oil and 2 to >4% (v/v) for chamomile oil. For enterococci the MIC values were significantly higher ranging from 0.25 to 1% (v/v), 0.5 to 2% (v/v), 1 to 4% (v/v), 4 to >4% (v/v) and >4% (v/v) for the above-mentioned oils, respectively. The main compounds of the tested essential oils were: estragole (Ocimum basilicum), bisabolol and trans-b-farnesene (Matricaria chamomilla), carvacrol and thymol (Thymus capitatus), terpinen-4-ol and p-cymene (Melaleuca alternifolia), thymol, linalool, and p-cymene (Thymus vulgaris). Origanum essential oil yielded the best antimicrobial results followed by thyme, tea tree, and basil oil, while chamomile oil exhibited weak antibacterial properties.

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“…Although previous work has demonstrated baseline high levels of specific AMR genes (63) and phenotypic resistance in E.coli isolates (33, 64) in unmedicated pigs, our initial expectation was that AMR gene abundances would markedly increase in response to antimicrobial administration as a result of selective pressure being exerted on specific gene subsets (65). In agreement with previous work, we showed high levels of all studied AMR genes in the non-medicated sow barn population, whilst prolonged exposure to three different in-feed antimicrobial regimens had no marked effect on AMR gene counts, potentially suggesting that they have reached saturation within the faecal bacterial populations (65). Curiously, the antimicrobials used (chlortetracycline and tylosin) were still clinically effective on this farm, suggesting that despite a high abundance of resistance genes within the faecal microbiome, that they were not present, or at least not active, within the organisms of clinical interest, i.e.…”

Section: Discussionmentioning

confidence: 95%

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 antimicrobial resistance crisis: management through gene monitoring

Cited by 7 publications

References 49 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

Antibacterial Efficacy of Commercially Available Essential Oils Tested Against Drug-Resistant Gram-Positive Pathogens

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

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