Antimicrobial use and production system shape the fecal, environmental, and slurry resistomes of pig farms

Mencía-Ares, Oscar; Cabrera‐Rubio, Raúl; Cobo‐Díaz, José F.; Álvarez‐Ordóñez, Avelino; Gómez‐García, Manuel; Puente, Héctor; Cotter, Paul D.; Crispie, Fiona; Carvajal, Ana; Rubio, Pedro; Argüello, Héctor

doi:10.1186/s40168-020-00941-7

Cited by 45 publications

(46 citation statements)

References 58 publications

(75 reference statements)

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“…22,Moor,submitted It is perhaps also relevant that we did not find any influence of antimicrobial treatments on the gut microbiota of pigs, which is a topic of controversy in the literature. 32,33 It has to be taken into consideration that our study was not well powered and different antimicrobials were administered which prevents drawing a final conclusion concerning the influence of antimicrobial substances on the gut microbiota of pigs.…”

Section: Discussionmentioning

confidence: 99%

Influence of pig farming on human Gut Microbiota: role of airborne microbial communities

et al. 2021

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It has been hypothesized that both genetics and diet influence the composition of the human cecal microbiota. However, it remains unclear whether and how occupational exposure to microbes impacts the microbial communities in human guts. Using a One Health approach, we visited pig farms (n = 26) and collected stool specimens from pig workers (n = 59), pig barn air samples (n = 19), and rectal swabs from pigs at three different growth stages (n = 144). Stool samples from cattle workers were included as a control group (n = 22). Each sample's microbiota was characterized using 16S rRNA gene sequencing and the DADA2 pipeline.We obtained a significantly different clustering of the microbial compositions of pig and cattle workers by permutational multivariate analysis of variance (PERMANOVA; P < .001). Workers primarily exposed to pigs had higher relative abundances of Prevotellaceae and less Bacteroidaceae than workers exposed to cattle. We also found that the microbial compositions of pig workers' stool samples shared extensive fractions with the samples from their pigs. We also identified amplicon sequencing variants (ASVs) in the airborne microbiota which were likely involved in zoonotic transmission events.We hypothesize that ASVs originating from pig feces are aerosolized and, through breathing, get trapped in the pig farm workers' upper respiratory tract from where they can get swallowed. Consequently, some of the animal associated ASVs are transferred into the gastrointestinal tracts (GITs) which leads to changes in the composition of the human gut microbiota. The importance of this finding for human health must be investigated further.

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Section: Discussionmentioning

confidence: 99%

Influence of pig farming on human Gut Microbiota: role of airborne microbial communities

et al. 2021

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“… [ 127 ] Feces ( n = 38) Yes NS –Predominant by tetracycline, followed by aminoglycosides, MLS, and oxazolidinones. [ 128 ] Ileum ( n = 23) and colon content ( n = 24) Yes Chlortetracycline and virginiamycin –No significant difference in the structure and diversity of ARGs and MGE after administration of low-dose antimicrobials. –Predominant by tetracycline, followed by macrolide, aminoglycoside, lincosamide, and streptogramin in colon.…”

Section: Introductionmentioning

confidence: 99%

A review of the resistome within the digestive tract of livestock

McAllister²,

Guan

2021

J Animal Sci Biotechnol

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Antimicrobials have been widely used to prevent and treat infectious diseases and promote growth in food-production animals. However, the occurrence of antimicrobial resistance poses a huge threat to public and animal health, especially in less developed countries where food-producing animals often intermingle with humans. To limit the spread of antimicrobial resistance from food-production animals to humans and the environment, it is essential to have a comprehensive knowledge of the role of the resistome in antimicrobial resistance (AMR), The resistome refers to the collection of all antimicrobial resistance genes associated with microbiota in a given environment. The dense microbiota in the digestive tract is known to harbour one of the most diverse resistomes in nature. Studies of the resistome in the digestive tract of humans and animals are increasing exponentially as a result of advancements in next-generation sequencing and the expansion of bioinformatic resources/tools to identify and describe the resistome. In this review, we outline the various tools/bioinformatic pipelines currently available to characterize and understand the nature of the intestinal resistome of swine, poultry, and ruminants. We then propose future research directions including analysis of resistome using long-read sequencing, investigation in the role of mobile genetic elements in the expression, function and transmission of AMR. This review outlines the current knowledge and approaches to studying the resistome in food-producing animals and sheds light on future strategies to reduce antimicrobial usage and control the spread of AMR both within and from livestock production systems.

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“…Recent international studies have characterised the pig faecal resistome (Xiao et al., 2016; Munk et al., 2018; Wang et al., 2019) or the EU farm environment (Luiken et al., 2020; Mencía‐Ares et al., 2020). ARGs in both dust and the farm environment are more diverse compared to the pig faecal resistome.…”

Section: Appendix F – Antimicrobial‐resistant Bacteria and Resistance Genes Of High Public Health Relevance In Environmental Sources Of Fmentioning

confidence: 99%

“…Scientific approaches need to move beyond surveys that simply identify ARB in the environment towards systematic and harmonised hypothesis‐driven investigations that definitively identify sources of AMR and selective agents for food‐producing environments, providing data that can be used to assess the risk to the food chain and public health. Such work should also identify interventions that can interrupt environmentally mediated pathways of AMR selection, acquisition and transmission and evaluate whether current and enhanced management practices and technologies to minimise environmental AMR contamination, especially for management of waste faecal material and water, can lead to desirable outcomes (Checcucci et al., 2020; Goulas et al., 2020; Mencía‐Ares et al., 2020; Ricker et al., 2020; Costa et al., 2021; Pereira et al., 2021; Radu et al., 2021; Youssef et al., 2021; Zhou et al., 2021).…”

Section: Assessmentmentioning

confidence: 99%

“…Outdoor production systems include organic production or extensive free‐range pig breeding and production. Outdoor farming is linked to a lower antimicrobial consumption and lower prevalence of ARB and ARGs (Österberg et al., 2006; Kempf et al., 2017; Mencía‐Ares et al., 2020). Despite the evident relevance of the environment, most of the current information relies on studies focused on faeces or intestinal contents.…”

Section: Appendix E – Sources and Transmission Routes Additional Information For Terrestrial Animals And Aquaculture Productionmentioning

confidence: 99%

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Role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain

Koutsoumanis¹,

Allende²,

Álvarez‐Ordóñez³

et al. 2021

EFS2

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The role of food-producing environments in the emergence and spread of antimicrobial resistance (AMR) in EU plant-based food production, terrestrial animals (poultry, cattle and pigs) and aquaculture was assessed. Among the various sources and transmission routes identified, fertilisers of faecal origin, irrigation and surface water for plant-based food and water for aquaculture were considered of major importance. For terrestrial animal production, potential sources consist of feed, humans, water, air/dust, soil, wildlife, rodents, arthropods and equipment. Among those, evidence was found for introduction with feed and humans, for the other sources, the importance could not be assessed. Several ARB of highest priority for public health, such as carbapenem or extended-spectrum cephalosporin and/or fluoroquinolone-resistant Enterobacterales (including Salmonella enterica), fluoroquinolone-resistant Campylobacter spp., methicillin-resistant Staphylococcus aureus and glycopeptide-resistant Enterococcus faecium and E. faecalis were identified. Among highest priority ARGs bla CTX-M , bla VIM , bla NDM , bla OXA-48like , bla OXA-23 , mcr, armA, vanA, cfr and optrA were reported. These highest priority bacteria and genes were identified in different sources, at primary and post-harvest level, particularly faeces/manure, soil and water. For all sectors, reducing the occurrence of faecal microbial contamination of fertilisers, water, feed and the production environment and minimising persistence/recycling of ARB within animal production facilities is a priority. Proper implementation of good hygiene practices, biosecurity and food safety management systems is very important. Potential AMR-specific interventions are in the early stages of development. Many data gaps relating to sources and relevance of transmission routes, diversity of ARB and ARGs, effectiveness of mitigation measures were identified. Representative epidemiological and attribution studies on AMR and its effective control in food production environments at EU level, linked to One Health and environmental initiatives, are urgently required.

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Antimicrobial use and production system shape the fecal, environmental, and slurry resistomes of pig farms

Cited by 45 publications

References 58 publications

Influence of pig farming on human Gut Microbiota: role of airborne microbial communities

Influence of pig farming on human Gut Microbiota: role of airborne microbial communities

A review of the resistome within the digestive tract of livestock

Role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain

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