An Environmental Science and Engineering Framework for Combating Antimicrobial Resistance

Pruden, Amy; Alcalde, Reinaldo E.; Alvarez, Pedro J. J.; Ashbolt, Nicholas J.; Bischel, Heather N.; Cápiro, Natalie L.; Crossette, Emily; Frigon, Dominic; Grimes, Kassandra L.; Haas, Charles N.; Ikuma, Kaoru; Kappell, Anthony D.; LaPara, Timothy M.; Kimbell, Lee K.; Li, Mengyan; Li, Xu; McNamara, Patrick J.; Seo, Young-Woo; Sobsey, Mark D.; Sozzi, Emanuele; Navab-Daneshmand, Tala; Raskin, Lutgarde; Riquelme, Maria V.; Vikesland, Peter J.; Wigginton, Krista; Zhou, Zhi

doi:10.1089/ees.2017.0520

Cited by 54 publications

(41 citation statements)

References 38 publications

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“…This highlights the potential to mine metagenomic data as a monitoring and assessment tool. One approach may be to search for specific ARG classes corresponding to critically important antibiotics (14). In the present study, several cephalosporin, MLS, colistin, quinolone, and glycopeptide ARGs were found, with some detectable in all fertilizer controls (e.g., OXA , SHV , erm , and vanHAX variants), whereas others ( KPC , qnrB , and qnrD ) were more sporadically detected (see Table S6 in the supplemental material).…”

Section: Discussionmentioning

confidence: 99%

“…The resulting sequence files were uploaded to MetaStorm (http://bench.cs.vt.edu/MetaStorm/) (53) and aligned to the Comprehensive Antibiotic Resistance Database (CARD v1.2.1) (14) (E value < 1e−10, identity > 80%, and ≥25 amino acids). DNA sequence reads were also compared to ARG-miner v1.1.6 (17), which includes ARGs from CARD (16), Antibiotic Resistance Genes Database (54), and UniProt, along with ARGs identified using a deep learning (deepARG) (18) algorithm and crowd-sourced annotation to keep it up to date.…”

Section: Methodsmentioning

confidence: 99%

“…Thus, there is a need to understand how various preharvest practices, such as application of manure-based amendments derived from cattle receiving antibiotics, will influence the variety of ARB and ARGs occurring on surfaces of fresh fruits and vegetables. Rather than focus on single strains or pathogens, a broad understanding of factors that mediate the potential for ARB and ARGs to evolve and spread through each stage of vegetable production is called for (14). A holistic “resistome” (15) framework in which the types and abundances of ARGs and gene transfer elements are comprehensively profiled via shotgun metagenomic sequencing holds promise for achieving this purpose.…”

Section: Introductionmentioning

confidence: 99%

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Effects of Dairy Manure-Based Amendments and Soil Texture on Lettuce- and Radish-Associated Microbiota and Resistomes

Guron

Arango-Argoty

Zhang

et al. 2019

mSphere

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Dairy cattle are routinely treated with antibiotics, and the resulting manure or composted manure is commonly used as a soil amendment for crop production, raising questions regarding the potential for antibiotic resistance to propagate from “farm to fork.” The objective of this study was to compare the microbiota and “resistomes” (i.e., carriage of antibiotic resistance genes [ARGs]) associated with lettuce leaf and radish taproot surfaces grown in different soils amended with dairy manure, compost, or chemical fertilizer only (control). Manure was collected from antibiotic-free dairy cattle (DC) or antibiotic-treated dairy cattle (DA), with a portion composted for parallel comparison. Amendments were applied to loamy sand or silty clay loam, and lettuce and radishes were cultivated to maturity in a greenhouse. Metagenomes were profiled via shotgun Illumina sequencing. Radishes carried a distinct ARG composition compared to that of lettuce, with greater relative abundance of total ARGs. Taxonomic species richness was also greater for radishes by 1.5-fold. The resistomes of lettuce grown with DC compost were distinct from those grown with DA compost, DC manure, or fertilizer only. Further, compost applied to loamy sand resulted in twofold-greater relative abundance of total ARGs on lettuce than when applied to silty clay loam. The resistomes of radishes grown with biological amendments were distinct from the corresponding fertilizer controls, but effects of composting or antibiotic use were not measureable. Cultivation in loamy sand resulted in higher species richness for both lettuce and radishes than when grown in silty clay loam by 2.2-fold and 1.2-fold, respectively, when amended with compost. IMPORTANCE A controlled, integrated, and replicated greenhouse study, along with comprehensive metagenomic analysis, revealed that multiple preharvest factors, including antibiotic use during manure collection, composting, biological soil amendment, and soil type, influence vegetable-borne resistomes. Here, radishes, a root vegetable, carried a greater load of ARGs and species richness than lettuce, a leafy vegetable. However, the lettuce resistome was more noticeably influenced by upstream antibiotic use and composting. Network analysis indicated that cooccurring ARGs and mobile genetic elements were almost exclusively associated with conditions receiving raw manure amendments, suggesting that composting could alleviate the mobility of manure-derived resistance traits. Effects of preharvest factors on associated microbiota and resistomes of vegetables eaten raw are worthy of further examination in terms of potential influence on human microbiomes and spread of antibiotic resistance. This research takes a step toward identifying on-farm management practices that can help mitigate the spread of agricultural sources of antibiotic resistance.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Effects of Dairy Manure-Based Amendments and Soil Texture on Lettuce- and Radish-Associated Microbiota and Resistomes

Guron

Arango-Argoty

Zhang

et al. 2019

mSphere

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“…The impact of the D parameter highlights that determining the actual dispersal rate of ARGs from the environment is crucial to understand the role of the environment in antibiotic resistance development. Comprehensive data on ARG dispersal would not only aid in risk assessment of emergence of novel resistance factors; it would also aid in understanding and mitigating the spread of resistant bacteria (and their ARGs) through the environment 6,8,10,38 .…”

Section: Discussionmentioning

confidence: 99%

What is the role of the environment in the emergence of novel antibiotic resistance genes? – A modelling approach

Bengtsson‐Palme

Jönsson

Heß

2021

Preprint

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It is generally accepted that intervention strategies to curb antibiotic resistance cannot solely focus on human and veterinary medicine but must also consider environmental settings. While the environment clearly has a role in the transmission of resistant bacteria, it is less clear what role it plays in the emergence of novel types of resistance. It has been suggested that the environment constitutes an enormous recruitment ground for resistance genes to pathogens, but the extent to which this actually happens is unknown. In this study, we built a model framework for resistance emergence and used the available quantitative data on the relevant processes to identify the steps which are limiting the appearance of antibiotic resistance determinants in human or animal pathogens. We also assessed the effect of uncertainty in the available data on the model results. We found that in a majority of scenarios, the environment would only play a minor role in the emergence of novel resistance genes. However, the uncertainty around this role is enormous, highlighting an urgent need of more quantitative data to understand the role of the environment in antibiotic resistance development. Specifically, more data is most needed on the fitness costs of antibiotic resistance gene (ARG) carriage, the degree of dispersal of resistant bacteria from the environment to humans, but also the rates of mobilization and horizontal transfer of ARGs. Quantitative data on these processes is instrumental to determine which processes that should be targeted for interventions to curb development and transmission of resistance.

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“…A solid comprehension of human activities' interaction with animals and the surrounding environment will help develop viable and sustainable solutions against the environmental emergency derived from the propagation and persistence of ARB and their genes. Considering the complexity of the problem, whether wastewater treatment contributes or not to the mitigation of antibiotic resistance is still a gap in the knowledge [62,63]. The WWTPs represent sites for amplification of ARB and ARGs and a valuable factor to mitigate the problem.…”

Section: Introductionmentioning

confidence: 99%

Treatment Processes for Microbial Resistance Mitigation: The Technological Contribution to Tackle the Problem of Antibiotic Resistance

Bairán

Rebollar-Pérez

Chávez

et al. 2020

IJERPH

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Advances generated in medicine, science, and technology have contributed to a better quality of life in recent years; however, antimicrobial resistance has also benefited from these advances, creating various environmental and health problems. Several determinants may explain the problem of antimicrobial resistance, such as wastewater treatment plants that represent a powerful agent for the promotion of antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARG), and are an important factor in mitigating the problem. This article focuses on reviewing current technologies for ARB and ARG removal treatments, which include disinfection, constructed wetlands, advanced oxidation processes (AOP), anaerobic, aerobic, or combined treatments, and nanomaterial-based treatments. Some of these technologies are highly intensive, such as AOP; however, other technologies require long treatment times or high doses of oxidizing agents. From this review, it can be concluded that treatment technologies must be significantly enhanced before the environmental and heath problems associated with antimicrobial resistance can be effectively solved. In either case, it is necessary to achieve total removal of bacteria and genes to avoid the possibility of regrowth given by the favorable environmental conditions at treatment plant facilities.

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An Environmental Science and Engineering Framework for Combating Antimicrobial Resistance

Cited by 54 publications

References 38 publications

Effects of Dairy Manure-Based Amendments and Soil Texture on Lettuce- and Radish-Associated Microbiota and Resistomes

Effects of Dairy Manure-Based Amendments and Soil Texture on Lettuce- and Radish-Associated Microbiota and Resistomes

What is the role of the environment in the emergence of novel antibiotic resistance genes? – A modelling approach

Treatment Processes for Microbial Resistance Mitigation: The Technological Contribution to Tackle the Problem of Antibiotic Resistance

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