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

Microbiome ◽  
2020 ◽  
Vol 8 (1) ◽  
Author(s):  
Oscar Mencía-Ares ◽  
Raúl Cabrera-Rubio ◽  
José Francisco Cobo-Díaz ◽  
Avelino Álvarez-Ordóñez ◽  
Manuel Gómez-García ◽  
...  

Abstract Background The global threat of antimicrobial resistance (AMR) is a One Health problem impacted by antimicrobial use (AMU) for human and livestock applications. Extensive Iberian swine production is based on a more sustainable and eco-friendly management system, providing an excellent opportunity to evaluate how sustained differences in AMU impact the resistome, not only in the animals but also on the farm environment. Here, we evaluate the resistome footprint of an extensive pig farming system, maintained for decades, as compared to that of industrialized intensive pig farming by analyzing 105 fecal, environmental and slurry metagenomes from 38 farms. Results Our results evidence a significantly higher abundance of antimicrobial resistance genes (ARGs) on intensive farms and a link between AMU and AMR to certain antimicrobial classes. We observed differences in the resistome across sample types, with a higher richness and dispersion of ARGs within environmental samples than on those from feces or slurry. Indeed, a deeper analysis revealed that differences among the three sample types were defined by taxa-ARGs associations. Interestingly, mobilome analyses revealed that the observed AMR differences between intensive and extensive farms could be linked to differences in the abundance of mobile genetic elements (MGEs). Thus, while there were no differences in the abundance of chromosomal-associated ARGs between intensive and extensive herds, a significantly higher abundance of integrons in the environment and plasmids, regardless of the sample type, was detected on intensive farms. Conclusions Overall, this study shows how AMU, production system, and sample type influence, mainly through MGEs, the profile and dispersion of ARGs in pig production.

Author(s):  
John W. Schmidt ◽  
Amit Vikram ◽  
Enrique Doster ◽  
Kevin Thomas ◽  
Margaret D Weinroth ◽  
...  

Antibiotics used during food-animal production account for approximately 77% of U.S. antimicrobial consumption by mass. Ground beef products labeled as raised without antibiotics (RWA) are perceived to harbor lower antimicrobial resistance (AMR) levels than conventional (CONV) products with no label claims regarding antimicrobial use. Retail ground beef samples were obtained from 6 U. S. cities. Samples with a RWA or USDA Organic claim ( N = 299) were assigned to the RWA production system. Samples lacking these claims ( N = 300) were assigned to the CONV production system. Each sample was cultured for the detection of five antimicrobial resistant bacteria. Genomic DNA was isolated from each sample and qPCR was used to determine the abundance of ten antimicrobial resistance genes (ARGs). Tetracycline-resistant Escherichia coli (CONV = 46.3%; RWA = 34.4%, P < 0.01) and erythromycin-resistant Enterococcus (CONV = 48.0%; RWA = 37.5%, P = 0.01) were more frequently detected in CONV. Salmonella were detected in 1.2% of samples. The ARG bla CTX-M (CONV = 4.1 log 10 normalized abundance, RWA = 3.8 log 10 normalized abundance, P < 0.01) was more abundant in CONV ground beef. The ARGs mecA (CONV = 4.4 log 10 normalized abundance, RWA = 4.9 log 10 normalized abundance, P = 0.05), tet (A) (CONV = 3.9 log 10 normalized abundance, RWA = 4.5 log 10 normalized abundance, P < 0.01), tet (B) (CONV = 3.9 log 10 normalized abundance, RWA = 4.5 log 10 normalized abundance, P < 0.01), and tet (M) (CONV = 5.4 log 10 normalized abundance, RWA = 5.8 log 10 normalized abundance, P < 0.01) were more abundant in RWA ground beef. Although these results suggest that antimicrobial use during U. S. cattle production does not increase human exposure to AMR via ground beef quantitative microbiological risk assessments are required for authoritative assessments regarding the human health impacts of antimicrobial uses during beef production.


2020 ◽  
Vol 15 (1) ◽  
Author(s):  
Dipti W. Pitta ◽  
Nagaraju Indugu ◽  
John D. Toth ◽  
Joseph S. Bender ◽  
Linda D. Baker ◽  
...  

Abstract Background Antimicrobial resistance is a serious concern. Although the widespread use of antimicrobials in livestock has exacerbated the emergence and dissemination of antimicrobial resistance genes (ARG) in farm environments, little is known about whether antimicrobial use affects distribution of ARG in livestock systems. This study compared the distribution of microbiomes and resistomes (collections of ARG) across different farm sectors in dairy herds that differed in their use of antimicrobials. Feces from heifers, non-lactating, and lactating cows, manure storage, and soil from three conventional (antimicrobials used to treat cows) and three organic (no antimicrobials used for at least four years) farms in Pennsylvania were sampled. Samples were extracted for genomic DNA, processed, sequenced on the Illumina NextSeq platform, and analyzed for microbial community and resistome profiles using established procedures. Results Microbial communities and resistome profiles clustered by sample type across all farms. Overall, abundance and diversity of ARG in feces was significantly higher in conventional herds compared to organic herds. The ARG conferring resistance to betalactams, macrolide-lincosamide-streptogramin (MLS), and tetracyclines were significantly higher in fecal samples of dairy cows from conventional herds compared to organic herds. Regardless of farm type, all manure storage samples had greater diversity (albeit low abundance) of ARG conferring resistance to aminoglycosides, tetracyclines, MLS, multidrug resistance, and phenicol. All soil samples had lower abundance of ARG compared to feces, manure, and lagoon samples and were comprised of ARG conferring resistance to aminoglycosides, glycopeptides, and multi-drug resistance. The distribution of ARG is likely driven by the composition of microbiota in the respective sample types. Conclusions Antimicrobial use on farms significantly influenced specific groups of ARG in feces but not in manure storage or soil samples.


2019 ◽  
Vol 3 (2) ◽  
Author(s):  
J. W. Schmidt ◽  
A. Vikram ◽  
K. Thomas ◽  
T. M. Arthur ◽  
M. Weinroth ◽  
...  

ObjectivesThe occurrences of human bacterial infections complicated by antimicrobial resistance (AMR) have increased in recent decades. Concerns have been raised that food-animal production practices that incorporate antimicrobials contribute significantly to human AMR exposures since food-animal production accounts for approximately 81% of U.S. antimicrobial consumption by mass. Although empirical studies comparing AMR levels in meat products, including ground beef, are scant ground beef products with Raised without Antibiotics (RWA) label claims are perceived to harbor less AMR than “conventional” (CONV) products with no label claims regarding antimicrobial use. The objective of this research was to determine AMR levels in retail ground beef with and without an RWA label claims.Materials and MethodsRetail ground beef samples were obtained from 6 U.S. cities. Samples were obtained on the following dates: 9/18/2017, 10/30/2017, 11/27/2017. 1/29/2018. 3/5/2018, and 6/11/2018. A total of 599 samples were obtained. Samples with a “Raised without Antibiotics” or USDA Organic claim (N = 299) were assigned to the RWA production system. Samples lacking a “Raised without Antibiotics” claim (N = 300) were assigned to the CONV production system. Each sample was cultured for the detection of five antimicrobial resistant bacteria (ARB). Genomic DNA was isolated from each sample and qPCR was used to determine the abundance of ten antimicrobial resistance genes (ARGs). The impacts of production system and city on ARB detection were assessed by the Likelihood-ratio chi-squared test. The impacts of production system and city on ARG abundance was assessed by two-way ANOVA.ResultsTetracycline-resistant Escherichia coli (CONV = 46.3%; RWA = 34.4%) and erythromycin-resistant Enterococcus (CONV = 48.0%; RWA = 37.5%) were more frequently (P < 0.01) detected in CONV. Detection of third generation cephalosporin-resistant E. coli (CONV = 5.7%; RWA = 1.0%), vancomycin-resistant Enterococcus (CONV = 0.0%; RWA = 0.0%) and methicillin-resistant Staphylococcus aureus (CONV = 1.3%; RWA = 0.7%) did not differ (P = 1.00). The blaCTX-M ARG was more abundant in CONV (2.4 vs. 2.1 log copies/gram, P = 0.01) but the tet(A) (2.4 vs. 2.5 log copies/gram, P = 0.02) and tet(M) (3.6 vs. 3.9 log copies/gram, P < 0.01) ARGs were more abundant in RWA. aadA1, blaCMY-2, mecA, erm(B), and tet(B) abundances did not differ significantly (Fig. 5) (P > 0.05). Abundances of aac (6’)-Ie-aph (2”)-Ia and blaKPC-2 were not analyzed since they were quantified in less than 5% of the samples.ConclusionU.S. retail CONV and RWA ground beef harbor generally similar levels of AMR since only 5 of 15 AMR measurements were statistically different between production systems. Three AMR measurements were higher in CONV, while 2 AMR measurements were higher in RWA. These results are in general agreement with a recently published study authored by our group that examined antimicrobial resistance in CONV and RWA ground beef obtained from U.S. foodservice suppliers (Vikram et al., J. Food Prot. 81:2007–2018. 2018.). Together these studies suggest that antimicrobial use during U.S. cattle production has minimal to no impact on human exposure to AMR via ground beef.Figure 5.


2020 ◽  
Vol 32 ◽  
Author(s):  
Juliana Alves Resende ◽  
Vânia Lúcia da Silva ◽  
Claudio Galuppo Diniz

Abstract: From an anthropocentric perspective, aquatic environments are important to maintain health and survival, however, as they are sometimes managed based on misconception, they are considered a convergent pathway for anthropogenic residues and sanitation. Thus, it is observed that these ecosystems have been threatened by chemical pollution due to xenobiotics, especially from a more contemporary approach, by the selective pressure associated with antimicrobials. There are several studies that report the enrichment of antimicrobial resistant bacteria and mobilizable antimicrobial resistance genes in aquatic and adjacent ecosystems. From the perspective of the emerging and reemerging number of diseases related to the interplay of human, animal, and environmental factors, a new conception arose to address these issues holistically, which is known as the One Health approach. Scientific and political discourse on this conception should lead to effective action plans for preventing and controlling the spread of infectious diseases in open environment, including those impacted by anthropogenic activities. Therefore, nowadays, discussions on antimicrobial resistance are becoming broader and are requiring a multi-disciplinary view to address health and environmental challenges, which includes aquatic environment management. Water may represent one of the most important ecosystems for the in antimicrobial resistance phenomenon that arises when a dynamic and singular microbial community may be influenced by several characteristics. As antimicrobial substances do not all degrade at the same time under the same treatment, strategies concerning their removal from the environment should consider their individualized chemical characteristics.


2021 ◽  
Author(s):  
Lu Yang ◽  
Yingbo Shen ◽  
Junyao Jiang ◽  
Xueyang Wang ◽  
Dongyan Shao ◽  
...  

Abstract Antimicrobial agents have been used in meat production for decades and its consumption is considered an key driver for the emergence and dissemination of antimicrobial resistance (AMR). However, large-scale studies on AMR changes in animal isolates since the introduction of antimicrobial usage remain scarce. We applied whole genome sequencing analysis to 982 animal-derived Escherichia coli collected in China from 1970s to 2019 and found increasing trends for the presence of numerous antimicrobial resistance genes (ARGs), including those conferring resistance to critically important agents for veterinary (florfenicol and norfloxacin) and human medicine (colistin, cephalosporins, and meropenem). Extensive diversity and increasing complexity of ARGs and their associated mobile genetic elements (MGEs) such as plasmids were also observed. The plasmids, IncC, IncHI2, IncK, IncI, IncX and IncF played a key role as highly effective vehicles for disseminating ARGs. Correlation analysis also revealed an association between antimicrobial production and emergence of ARGs at a spatial and temporal level. Prohibiting or strictly curtailing antimicrobial use in animals will potentially negate the current trends of AMR as the bacterial genome is highly changeable and using different drugs of the same class, or even unrelated classes, may co-select for MGEs carrying a plethora of co-existing ARGs. Therefore, limiting or ceasing antimicrobial use in animals to control AMR requires careful consideration.


2021 ◽  
Vol 3 (1) ◽  
Author(s):  
Adrián López-Catalina ◽  
Raquel Atxaerandio ◽  
Aser García-Rodríguez ◽  
Idoia Goiri ◽  
Mónica Gutierrez-Rivas ◽  
...  

Abstract Background Rumen microorganisms carry antimicrobial resistance genes which pose a threaten to animals and humans in a One Health context. In order to tackle the emergence of antimicrobial resistance it is vital to understand how they appear, their relationship with the host, how they behave as a whole in the ruminal ecosystem or how they spread to the environment or humans. We sequenced ruminal samples from 416 Holstein dairy cows in 14 Spanish farms using nanopore technology, to uncover the presence of resistance genes and their potential effect on human, animal and environmental health. Results We found 998 antimicrobial resistance genes (ARGs) in the cow rumen and studied the 25 most prevalent genes in the 14 dairy cattle farms. The most abundant ARGs were related to the use of antibiotics to treat mastitis, metritis and lameness, the most common diseases in dairy cattle. The relative abundance (RA) of bacteriophages was positively correlated to the ARGs RA. The heritability of the RA of the more abundant ARGs ranged between 0.10 (mupA) and 0.49 (tetW), similar to the heritability of the RA of microbes that carried those ARGs. Even though these genes are carried by the microorganisms, the host is partially controlling their RA by having a more suitable rumen pH, folds, or other physiological traits that promote the growth of those microorganisms. Conclusions We were able to determine the most prevalent ARGs (macB, msbA, parY, rpoB2, tetQ and TaeA) in the ruminal bacteria ecosystem. The rumen is a reservoir of ARGs, and strategies to reduce the ARG load from livestock must be pursued.


2020 ◽  
Vol 33 (3) ◽  
Author(s):  
David M. P. De Oliveira ◽  
Brian M. Forde ◽  
Timothy J. Kidd ◽  
Patrick N. A. Harris ◽  
Mark A. Schembri ◽  
...  

SUMMARY Antimicrobial-resistant ESKAPE (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species) pathogens represent a global threat to human health. The acquisition of antimicrobial resistance genes by ESKAPE pathogens has reduced the treatment options for serious infections, increased the burden of disease, and increased death rates due to treatment failure and requires a coordinated global response for antimicrobial resistance surveillance. This looming health threat has restimulated interest in the development of new antimicrobial therapies, has demanded the need for better patient care, and has facilitated heightened governance over stewardship practices.


2019 ◽  
Vol 4 (1) ◽  
pp. 22 ◽  
Author(s):  
Peter Collignon ◽  
Scott McEwen

Approaching any issue from a One Health perspective necessitates looking at the interactions of people, domestic animals, wildlife, plants, and our environment. For antimicrobial resistance this includes antimicrobial use (and abuse) in the human, animal and environmental sectors. More importantly, the spread of resistant bacteria and resistance determinants within and between these sectors and globally must be addressed. Better managing this problem includes taking steps to preserve the continued effectiveness of existing antimicrobials such as trying to eliminate their inappropriate use, particularly where they are used in high volumes. Examples are the mass medication of animals with critically important antimicrobials for humans, such as third generation cephalosporins and fluoroquinolones, and the long term, in-feed use of antimicrobials, such colistin, tetracyclines and macrolides, for growth promotion. In people it is essential to better prevent infections, reduce over-prescribing and over-use of antimicrobials and stop resistant bacteria from spreading by improving hygiene and infection control, drinking water and sanitation. Pollution from inadequate treatment of industrial, residential and farm waste is expanding the resistome in the environment. Numerous countries and several international agencies have now included a One Health Approach within their action plans to address antimicrobial resistance. Necessary actions include improvements in antimicrobial use, better regulation and policy, as well as improved surveillance, stewardship, infection control, sanitation, animal husbandry, and finding alternatives to antimicrobials.


2018 ◽  
Vol 81 (12) ◽  
pp. 2007-2018 ◽  
Author(s):  
AMIT VIKRAM ◽  
ERIC MILLER ◽  
TERRANCE M. ARTHUR ◽  
JOSEPH M. BOSILEVAC ◽  
TOMMY L. WHEELER ◽  
...  

ABSTRACTU.S. ground beef with “raised without antibiotics” (RWA) label claims are perceived as harboring fewer bacteria with antimicrobial resistance (AMR) than are found in conventional (CONV) ground beef with no such label claim. A total of 370 ground beef samples from CONV (n = 191) and RWA (n = 179) production systems were collected over 13 months from three food service suppliers. The following bacteria were cultured: Escherichia coli, tetracycline-resistant (TETr) E. coli, third-generation cephalosporin-resistant (3GCr) E. coli, Salmonella enterica, TETr S. enterica, 3GCr S. enterica, nalidixic acid–resistant S. enterica, Enterococcus spp., erythromycin-resistant Enterococcus spp., TETr Enterococcus spp., Staphylococcus aureus, and methicillin-resistant S. aureus. TETr E. coli was more frequently detected in CONV ground beef (CONV, 54.2%; RWA, 35.2%; P &lt; 0.01), but supplier (P &lt; 0.01) and production system × suppler interaction (P &lt; 0.01) effects were also significant. Metagenomic DNA was isolated from each sample, and equal amounts of metagenomic DNA were pooled by supplier, month, and production system for 75 pooled samples (38 CONV, 37 RWA). The abundance of aac(6′)-Ie-aph(2″)-Ia, aadA1, blaCMY-2, blaCTX-M, blaKPC-2, erm(B), mecA, tet(A), tet(B), and tet(M) genes was assessed by quantitative PCR. The tet(A) (2.9-log2-fold change, P = 0.04) and tet(B) (5.6-log2-fold change) (P = 0.03) genes were significantly more abundant in RWA ground beef. Phylogenetic analyses revealed that ground beef microbiomes differed more by supplier than by production system. These results were consistent with prior research suggesting antimicrobial use in U.S. beef cattle has minimal impact on the AMR of bacteria found in these products. These results should spur a reevaluation of assumptions regarding the impact of antimicrobial use during U.S. beef production on the AMR of bacteria in ground beef.


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