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      Antibiotic use on crops in low and middle-income countries based on recommendations made by agricultural advisors

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      1 , a , , 1
      CABI Agriculture and Bioscience
      BioMed Central
      Antibiotics, Antibiotic resistance, Crop protection, Plant clinics, Plantwise, LMIC, Agricultural-advisors, Extension

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          Abstract

          Background

          Microbial resistance to medically important antibiotics is of international concern. There is considerable attention paid to the medical and veterinary use of antibiotics but there is a paucity of data on their use in global crop production. The only well documented use of antibiotics on crops is that on top fruit in the USA. Due to the absence of other data it is generally assumed that this use comprises the bulk of antibiotics applied to plants. The goal of this study was to investigate the scale and diversity of antibiotics being recommended for managing crop health problems in LMICs and the crops and types of problems for which they are selected.

          Methods

          Plantwise is an international program which assists with the provision of agronomic advice to smallholder farmers in LMICs. Recommendations relating to the management of crop problems are stored in an international database, comprising over 400,000 records collected over 8 years. The extent of antibiotic use in crop production when grouped by the WHO regions was analysed using descriptive statistics.

          Results

          Within our data all WHO regions of the world are using antibiotics on crop plants with the exception of Africa (no data for Europe) and the main crop on which they are used is rice. In some years, and in one region, nearly 10% of the management recommendations for rice contained an antibiotic. Eleven antibiotics are being recommended on crops (often blended together) and there is considerable regional variation as to where they are used. The problems against which antibiotics are recommended are extremely varied and we speculate that they are often used as a prophylactic spray to prevent, or control, low levels of bacterial disease.

          Conclusions

          The data reveals that antibiotics are being recommended far more frequently and on a much greater variety of crops than previously thought. Relative to medical and veterinary use the quantities used globally are comparatively small, but this niche does provide some unique avenues by which resistance could develop in human pathogens. Results presented here have implications for those wanting to limit the spread of antibiotic resistance.

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          Most cited references36

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          Global trends in antimicrobial use in food animals.

          Demand for animal protein for human consumption is rising globally at an unprecedented rate. Modern animal production practices are associated with regular use of antimicrobials, potentially increasing selection pressure on bacteria to become resistant. Despite the significant potential consequences for antimicrobial resistance, there has been no quantitative measurement of global antimicrobial consumption by livestock. We address this gap by using Bayesian statistical models combining maps of livestock densities, economic projections of demand for meat products, and current estimates of antimicrobial consumption in high-income countries to map antimicrobial use in food animals for 2010 and 2030. We estimate that the global average annual consumption of antimicrobials per kilogram of animal produced was 45 mg⋅kg(-1), 148 mg⋅kg(-1), and 172 mg⋅kg(-1) for cattle, chicken, and pigs, respectively. Starting from this baseline, we estimate that between 2010 and 2030, the global consumption of antimicrobials will increase by 67%, from 63,151 ± 1,560 tons to 105,596 ± 3,605 tons. Up to a third of the increase in consumption in livestock between 2010 and 2030 is imputable to shifting production practices in middle-income countries where extensive farming systems will be replaced by large-scale intensive farming operations that routinely use antimicrobials in subtherapeutic doses. For Brazil, Russia, India, China, and South Africa, the increase in antimicrobial consumption will be 99%, up to seven times the projected population growth in this group of countries. Better understanding of the consequences of the uninhibited growth in veterinary antimicrobial consumption is needed to assess its potential effects on animal and human health.
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            Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential

            Background Antibacterial biocides and metals can co-select for antibiotic resistance when bacteria harbour resistance or tolerance genes towards both types of compounds. Despite numerous case studies, systematic and quantitative data on co-occurrence of such genes on plasmids and chromosomes is lacking, as is knowledge on environments and bacterial taxa that tend to carry resistance genes to such compounds. This effectively prevents identification of risk scenarios. Therefore, we aimed to identify general patterns for which biocide/metal resistance genes (BMRGs) and antibiotic resistance genes (ARGs) that tend to occur together. We also aimed to quantify co-occurrence of resistance genes in different environments and taxa, and investigate to what extent plasmids carrying both types of genes are conjugative and/or are carrying toxin-antitoxin systems. Results Co-occurrence patterns of resistance genes were derived from publicly available, fully sequenced bacterial genomes (n = 2522) and plasmids (n = 4582). The only BMRGs commonly co-occurring with ARGs on plasmids were mercury resistance genes and the qacE∆1 gene that provides low-level resistance to quaternary ammonium compounds. Novel connections between cadmium/zinc and macrolide/aminoglycoside resistance genes were also uncovered. Several clinically important bacterial taxa were particularly prone to carry both BMRGs and ARGs. Bacteria carrying BMRGs more often carried ARGs compared to bacteria without (p < 0.0001). BMRGs were found in 86 % of bacterial genomes, and co-occurred with ARGs in 17 % of the cases. In contrast, co-occurrences of BMRGs and ARGs were rare on plasmids from all external environments (<0.7 %) but more common on those of human and domestic animal origin (5 % and 7 %, respectively). Finally, plasmids with both BMRGs and ARGs were more likely to be conjugative (p < 0.0001) and carry toxin-antitoxin systems (p < 0.0001) than plasmids without resistance genes. Conclusions This is the first large-scale identification of compounds, taxa and environments of particular concern for co-selection of resistance against antibiotics, biocides and metals. Genetic co-occurrences suggest that plasmids provide limited opportunities for biocides and metals to promote horizontal transfer of antibiotic resistance through co-selection, whereas ample possibilities exist for indirect selection via chromosomal BMRGs. Taken together, the derived patterns improve our understanding of co-selection potential between biocides, metals and antibiotics, and thereby provide guidance for risk-reducing actions. Electronic supplementary material The online version of this article (doi:10.1186/s12864-015-2153-5) contains supplementary material, which is available to authorized users.
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              Antibiotic Resistance in Plant-Pathogenic Bacteria

              Antibiotics have been used for the management of relatively few bacterial plant diseases and are largely restricted to high-value fruit crops because of the expense involved. Antibiotic resistance in plant-pathogenic bacteria has become a problem in pathosystems where these antibiotics have been used for many years. Where the genetic basis for resistance has been examined, antibiotic resistance in plant pathogens has most often evolved through the acquisition of a resistance determinant via horizontal gene transfer. For example, the strAB streptomycin-resistance genes occur in Erwinia amylovora, Pseudomonas syringae, and Xanthomonas campestris, and these genes have presumably been acquired from nonpathogenic epiphytic bacteria colocated on plant hosts under antibiotic selection. We currently lack knowledge of the effect of the microbiome of commensal organisms on the potential of plant pathogens to evolve antibiotic resistance. Such knowledge is critical to the development of robust resistance management strategies to ensure the safe and effective continued use of antibiotics in the management of critically important diseases.
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                Author and article information

                Journal
                ab
                CABI Agriculture and Bioscience
                BioMed Central (London )
                2662-4044
                23 June 2020
                December 2020
                : 1
                : 1
                : 1
                Affiliations
                [1 ] org-nameCABI-EUK Bakeham Lane; TW209TY Egham UK
                Author notes
                Author information
                http://orcid.org/0000-0003-1741-4595
                Article
                s43170-020-00001-y 1
                10.1186/s43170-020-00001-y
                e7b7c980-339b-4d66-9e7a-480529f132df
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 30 March 2020
                : 16 January 2020
                : 30 March 2020
                : 23 June 2020
                Categories
                Research Article
                Environmental and soil science
                Plant pathology
                Food security and nutrition
                ab, CABI Agriculture and Bioscience
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                BioMed Central
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                Life Sciences
                Agriculture
                Biomedical and Life Sciences
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                Plantwise,Plant clinics,Crop protection,Antibiotic resistance,Antibiotics,Extension,Agricultural-advisors,LMIC

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