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

Abstract

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 ...

Antimicrobial use in wean to market pigs in the United States assessed via voluntary sharing of proprietary data

“…Tetracyclines were among the earliest antimicrobials used in food animal production (Jukes, 1985) and have multiple approved label claims for administration via feed, water and injection to swine in the United States. Although tetracycline resistance (phenotypically and genotypically) is prevalent in some pathogens and commensal bacteria of swine (Hayer et al., 2020a, 2020b; Holmer et al., 2019), this class appears to remain clinically valuable and widely used, even in herds where tetracycline resistance genes are abundant across the microbiome (Pollock et al., 2020). With respect to critically important antimicrobials, most concern regarding human health has surrounded the use in food animals of fluoroquinolones (e.g.…”

Mapping Microbiome Signatures Associated With Antibiotic Usage On A Swine Production Farm Using Amplicon And Shotgun Data

“…Dry sows (Nontreated group) were housed in straw yards (referred to as the "sow barn") and nursing sows and piglets were housed on slats. Detailed herd and antimicrobial usage records have been published in our previous work [11].…”

“…However, there are few longitudinal studies that have interrogated AMR gene generation and dissemination in livestock production systems to date. Such approaches are essential to disentangle the contribution of temporal and contextual microbiome variation in high antibiotic use systems such as swine production [11]. Our previous work [11] indicated a state of saturation of AMR genes in a swine production system, with no apparent impact on the utility of antibiotics to limit infections and mortality.…”

“…Such approaches are essential to disentangle the contribution of temporal and contextual microbiome variation in high antibiotic use systems such as swine production [11]. Our previous work [11] indicated a state of saturation of AMR genes in a swine production system, with no apparent impact on the utility of antibiotics to limit infections and mortality. Here, we seek to unravel the microbiome characteristics and the association with antimicrobial resistance genes, referred to as the resistome, in the pig faecal samples on this farm.…”

Alternatives to antibiotics in a One Health context and the role genomics can play in reducing antimicrobial use

“…Additionally, a higher-resolution understanding of microbiota dynamics is required. For example, the use of large-scale crosssectional [35] and longitudinal [36] microbiome data has linked the effects of antibiotic administration with AMR gene abundance and diversity in pig production systems. Specifically, metagenomic sequencing allows a comprehensive analysis of both microbial taxonomy and identification of genes encoding for antimicrobial resistance, toxin production and the presence of mobile genetic elements.…”