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Antimicrobial Stewardship in Food-Producing Animals

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Veterinary Microbiology".

Deadline for manuscript submissions: closed (31 July 2021) | Viewed by 24174

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Special Issue Editors

Dr. Paul Plummer

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Guest Editor

National Institute of Antimicrobial Resistance Research and Education, Ames, IA, USA
Interests: antimicrobial resistance; one health; veterinary; microbiology; bacteriology; zoonosis
Special Issues, Collections and Topics in MDPI journals

Dr. Derek Foster

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Guest Editor

Department of Population Health and Pathobiology, North Carolina State University, Raleigh, NC, USA
Interests: antimicrobial resistance; gastrointestinal disease; pharmacokinetics; veterinary

Special Issue Information

Dear Colleagues,

Antimicrobial stewardship collectively refers to the actions and decision making that antibiotic prescribers take to preserve the effectiveness and availability of antimicrobial drugs while working to optimize human, animal, and environmental health. In the context of livestock medicine, this oversight and decision making relies on veterinarians and the subsequent actions and decisions of farm workers implementing the plans developed by the veterinarian. In this Special Edition, we will focus on manuscripts that relate to antimicrobial stewardship in food-producing animals (livestock, poultry, and aquaculture). We encourage the submission of manuscripts that provide insights that can be translated into clinical practice. This includes contributions from basic science, social sciences, extension and education, and clinical medicine. Antimicrobial stewardship is about more than just the act of prescribing and involves identifying ways to decrease antibiotic use by:

Improving early detection of disease as a means of decreasing antibiotic use;
Preventing diseases generally treated with antibiotics;
Evaluating antibiotic alternatives;
Selecting and using antimicrobial judiciously;
Evaluating antimicrobial drug use practices

Dr. Paul Plummer
Dr. Derek Foster
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Microorganisms is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

antibiotics
antibiotic stewardship
livestock
antimicrobial resistance
poultry
aquaculture

Published Papers (10 papers)

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Research

22 pages, 2946 KiB

Open AccessArticle

Enrofloxacin Alters Fecal Microbiota and Resistome Irrespective of Its Dose in Calves

by Ashenafi Feyisa Beyi, Debora Brito-Goulart, Tyler Hawbecker, Brandon Ruddell, Alan Hassall, Renee Dewell, Grant Dewell, Orhan Sahin, Qijing Zhang and Paul J. Plummer

Microorganisms 2021, 9(10), 2162; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9102162 - 17 Oct 2021

Cited by 6 | Viewed by 2157

Abstract

Enrofloxacin is a fluoroquinolone drug used to prevent and control bovine respiratory disease (BRD) complex in multiple or single doses, ranging from 7.5 to 12.5 mg/kg body weight. Here, we examined the effects of high and low doses of a single subcutaneously injected enrofloxacin on gut microbiota and resistome in calves. Thirty-five calves sourced for this study were divided into five groups: control (n = 7), two low dose groups (n = 14, 7.5 mg/kg), and two high dose groups (n = 14, 12.5 mg/kg). One group in the low and high dose groups was challenged with Mannheimia haemolytica to induce BRD. Both alpha and beta diversities were significantly different between pre- and post-treatment microbial communities (q < 0.05). The high dose caused a shift in a larger number of genera than the low dose. Using metagenomic ProxiMeta Hi-C, 32 unique antimicrobial resistance genes (ARGs) conferring resistance to six antibiotic classes were detected with their reservoirs, and the high dose favored clonal expansion of ARG-carrying bacterial hosts. In conclusion, enrofloxacin treatment can alter fecal microbiota and resistome irrespective of its dose. Hi-C sequencing provides significant benefits for unlocking new insights into the ARG ecology of complex samples; however, limitations in sample size and sequencing depth suggest that further work is required to validate the findings. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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14 pages, 28474 KiB

Open AccessArticle

Incidence of Tetracycline and Erythromycin Resistance in Meat-Associated Bacteria: Impact of Different Livestock Management Strategies

by Cecilia Fontana, Vania Patrone, Constanza Maria Lopez, Lorenzo Morelli and Annalisa Rebecchi

Microorganisms 2021, 9(10), 2111; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9102111 - 07 Oct 2021

Cited by 12 | Viewed by 1874

Abstract

The extensive use of antibiotics as growth promoters, or their continued abusive misuse to cure or prevent the onset of bacterial infections as occurs in the intensive farming, may have played a pivotal role in the spread of reservoirs of antibiotic resistance (AR) among food-associated bacteria including pathogens representing risks to human health. The present study compares the incidence of tetracycline and erythromycin resistances in lactic acid bacteria (LAB) and coagulase negative staphylococci (CNS) from fermented products manufacturing using meat from intensive animal husbandry (industrialized manufacturing Italian salami) and from extensive farms (artisanal sausages facilities pork and llama Argentinean sausages). A higher incidence of tetracycline resistance (TET-R) compared to erythromycin resistance (ERY-R) was observed among the 205 isolates. Unlike CNS strains, the LAB showed a significant correlation between the TET-R and the ERY-R phenotypes. Genotypic assessment shows a high correlation with tetK and tetM for the TET-R strains and with ermB and ermC for the ERY-R strains. Multiple correspondence analyses have highlighted the association between AR phenotypes and CNS species isolated from Italian salami, while the susceptible phenotypes were associated with the LAB species from Argentinean sausages. Since antibiotic resistance in meat-associated bacteria is a very complex phenomenon, the assessment of bacterial resistance in different environmental contexts with diverse farming practices and food production technologies will help in monitoring the factors influencing AR emergence and spread in animal production. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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20 pages, 2253 KiB

Open AccessArticle

Estimating the Rates of Acquisition and loss of Resistance of Enterobacteriaceae to Antimicrobial Drugs in Pre-Weaned Dairy Calves

by Elisa Cella, Emmanuel Okello, Paul V. Rossitto, Beniamino T. Cenci-Goga, Luca Grispoldi, Deniece R. Williams, David B. Sheedy, Richard Pereira, Betsy M. Karle, Terry W. Lehenbauer and Sharif S. Aly

Microorganisms 2021, 9(10), 2103; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9102103 - 06 Oct 2021

Cited by 2 | Viewed by 1640

Abstract

The objective of this study was to investigate the effect of the antimicrobial drugs (AMD) on the shedding of resistant Enterobacteriaceae in feces of pre-weaned dairy calves. The AMD considered were ceftiofur, administered parenterally, and neomycin sulfate added in milk replacer and fed to calves during the first 20 days of life. Fifty-five calves, aged one to three days, were enrolled and followed to 64 days. Fecal samples were collected three times/week and treatments recorded daily. Enterobacteriaceae were quantified for a subset of 33 calves using spiral plating on plain, ceftiofur supplemented, and neomycin supplemented MacConkey agar. Negative binomial models were used to predict the association between treatment with AMD and the gain and loss of Enterobacteriaceae resistance over time. Acquisition of resistance by the Enterobacteriaceae occurred during treatment and peaked between days three to four post-treatment before decreasing to below treatment levels at days seven to eight post-treatment. Acquisition of neomycin resistance was observed on the first sampling day (day four from the start of feeding medicated milk replacer) to day eight, followed by cyclical peaks until day 29, when the Enterobacteriaceae counts decreased below pre-treatment. Enterobacteriaceae resistance against both AMD increased after AMD administration and didn’t return to pre-therapeutic status until seven or more days after therapy had been discontinued. The study findings provide valuable insights into the dynamics of Enterobacteriaceae under routine AMD use in calves. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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22 pages, 1610 KiB

Open AccessArticle

Danofloxacin Treatment Alters the Diversity and Resistome Profile of Gut Microbiota in Calves

by Ashenafi Feyisa Beyi, Debora Brito-Goulart, Tyler Hawbecker, Clare Slagel, Brandon Ruddell, Alan Hassall, Renee Dewell, Grant Dewell, Orhan Sahin, Qijing Zhang and Paul J. Plummer

Microorganisms 2021, 9(10), 2023; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9102023 - 24 Sep 2021

Cited by 6 | Viewed by 2641

Abstract

Fluoroquinolones, such as danofloxacin, are used to control bovine respiratory disease complex in beef cattle; however, little is known about their effects on gut microbiota and resistome. The objectives were to evaluate the effect of subcutaneously administered danofloxacin on gut microbiota and resistome, and the composition of Campylobacter in calves. Twenty calves were injected with a single dose of danofloxacin, and ten calves were kept as a control. The effects of danofloxacin on microbiota and the resistome were assessed using 16S rRNA sequencing, quantitative real-time PCR, and metagenomic Hi-C ProxiMeta. Alpha and beta diversities were significantly different (p < 0.05) between pre-and post-treatment samples, and the compositions of several bacterial taxa shifted. The patterns of association between the compositions of Campylobacter and other genera were affected by danofloxacin. Antimicrobial resistance genes (ARGs) conferring resistance to five antibiotics were identified with their respective reservoirs. Following the treatment, some ARGs (e.g., ant9, tet40, tetW) increased in frequencies and host ranges, suggesting initiation of horizontal gene transfer, and new ARGs (aac6, ermF, tetL, tetX) were detected in the post-treatment samples. In conclusion, danofloxacin induced alterations of gut microbiota and selection and enrichment of resistance genes even against antibiotics that are unrelated to danofloxacin. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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15 pages, 2194 KiB

Open AccessArticle

Comparison of the Intestinal Pharmacokinetics of Two Different Florfenicol Dosing Regimens and Its Impact on the Prevalence and Phenotypic Resistance of E. coli and Enterococcus over Time

by Jennifer L. Halleran, Ryker Minch, Hannah J. Slyvester, Megan E. Jacob, Timo Prange, Ronald Baynes and Derek M. Foster

Microorganisms 2021, 9(9), 1835; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9091835 - 30 Aug 2021

Cited by 3 | Viewed by 1764

Abstract

In order to mitigate the food animal sector’s role in the growing threat of antimicrobial resistance (AMR), the World Health Organization (WHO) suggests the use of lower tier antimicrobials, such as florfenicol. Florfenicol has two dosing schemes used to treat primarily bovine respiratory disease. In this study, the objective was to characterize the plasma and gastrointestinal pharmacokinetics of each dosing regimen and assess the effect of these dosing regimens on the prevalence of resistant indicator bacteria over time. Twelve steers underwent abdominal surgery to facilitate the placement of ultrafiltration probes within the lumen of the ileum and colon, as well as placement of an interstitial probe. Following surgery, cattle were dosed with either 20 mg/kg IM every 48 h of florfenicol given twice (n = 6) or a single, subcutaneous dose (40 mg/kg, n = 6). Plasma, interstitial fluid, gastrointestinal ultrafiltrate, and feces were collected. Pharmacokinetic analysis demonstrated high penetration of florfenicol within the gastrointestinal tract for both the high and low dose group (300%, 97%, respectively). There was no significant difference noted between dosing groups in proportion or persistence of phenotypically resistant bacterial isolates; however, the percent of resistant isolates was high throughout the study period. The recommendation for the use of a lower tier antimicrobial, such as florfenicol, may allow for the persistence of co-resistance for antibiotics of high regulatory concern. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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17 pages, 1166 KiB

Open AccessArticle

Comparison of Quantification Methods to Estimate Farm-Level Usage of Antimicrobials in Medicated Feed in Dairy Farms from Québec, Canada

by Hélène Lardé, David Francoz, Jean-Philippe Roy, Marie Archambault, Jonathan Massé, Marie-Ève Paradis and Simon Dufour

Microorganisms 2021, 9(9), 1834; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9091834 - 30 Aug 2021

Cited by 3 | Viewed by 2324

Abstract

Monitoring antimicrobial usage (AMU) in dairy cattle is becoming common in a growing number of countries, with the ultimate goal to improve practices, reduce the development of antimicrobial resistance, and protect human health. However, antimicrobials delivered as feed additives can be missed by some of the quantification methods usually implemented. Our objective was to compare three methods of quantification of in-feed AMU in Québec dairy herds. We recruited 101 dairy producers for one year in the Québec province. Quantities of antimicrobials were calculated by farm from: (1) feed mills invoices (reference method); (2) veterinary prescriptions; and (3) information collected during an in-person interview of each producer. We standardized AMU rates in kilograms per 100 cow-years and compared the reference method to both alternative methods using concordance correlation coefficients and Bland–Altman plots. Antimicrobial usage was well estimated by veterinary prescriptions (concordance correlation coefficient (CCC) = 0.66) or by the approximation using producer’s data (CCC = 0.73) when compared with actual deliveries by feed mills. Users of medically important antimicrobials for human medicine (less than 10% of the farms) were easily identified using veterinary prescriptions. Given that veterinary prescriptions were mostly electronic (90%), this method could be integrated as part of a monitoring system in Québec. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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37 pages, 11924 KiB

Open AccessArticle

2019 Survey of Antimicrobial Drug Use and Stewardship Practices in Adult Cows on California Dairies: Post Senate Bill 27

by Essam M. Abdelfattah, Pius S. Ekong, Emmanuel Okello, Deniece R. Williams, Betsy M. Karle, Joan D. Rowe, Edith S. Marshall, Terry W. Lehenbauer and Sharif S. Aly

Microorganisms 2021, 9(7), 1507; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9071507 - 14 Jul 2021

Cited by 9 | Viewed by 2235

Abstract

Antimicrobial resistance (AMR) is a global issue for both human and animal health. Antimicrobial drug (AMD) use in animals can contribute to the emergence of AMR. In January 2018, California (CA) implemented legislation (Senate Bill 27; SB 27) requiring veterinary prescriptions for medically important AMD use in food animals. The objective of our survey was to characterize AMD use, health management, and AMD stewardship practices of adult cows on CA dairies since the implementation of SB 27. In 2019, we mailed a questionnaire to 1282 California dairies. We received a total of 131 (10.2%) survey responses from 19 counties in CA. Our results showed that 45.6% of respondents included a veterinarian in their decision on which injectable AMD to purchase. Additionally, 48.8% of dairy producers included a veterinarian in their decision on which AMDs were used to treat sick cows. The majority (96.8%) of dairy producers were aware that all uses of medically important AMDs require a prescription. Approximately 49% of respondents agreed or strongly agreed that AMD use in livestock does not cause problems in humans. The survey documents antimicrobial use and stewardship practices in CA’s dairy industry and focus areas for future research and education. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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13 pages, 590 KiB

Open AccessArticle

Determination of Antimicrobial Resistance Patterns in Salmonella from Commercial Poultry as Influenced by Microbiological Culture and Antimicrobial Susceptibility Testing Methods

by Xi Wang, W. Evan Chaney, Hilary O. Pavlidis, James P. McGinnis, J. Allen Byrd, Yuhua Z. Farnell, Timothy J. Johnson, Audrey P. McElroy and Morgan B. Farnell

Microorganisms 2021, 9(6), 1319; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9061319 - 17 Jun 2021

Viewed by 2725

Abstract

Monitoring antimicrobial resistance of foodborne pathogens in poultry is critical for food safety. We aimed to compare antimicrobial resistance phenotypes in Salmonella isolated from poultry samples as influenced by isolation and antimicrobial susceptibility testing methods. Salmonella isolates were cultured from a convenience sample of commercial broiler ceca with and without selective broth enrichment, and resistance phenotypes were determined for 14 antimicrobials using the Sensititre^® platform and a qualitative broth breakpoint assay. The broth breakpoint method reported higher resistance to chloramphenicol, sulfisoxazole, and the combination of trimethoprim and sulfamethoxazole, and lower resistance to streptomycin as compared to the Sensititre^® assay in trial one. Selective enrichment of samples containing Salmonella in Rappaport-Vassiliadis broth reported lowered detectable resistance to amoxicillin/clavulanic acid, ampicillin, azithromycin, cefoxitin, ceftriaxone, nalidixic acid, and meropenem, and increased resistance to streptomycin and tetracycline than direct-plating samples in trial one. Using matched isolates in trial two, the Sensititre^® assay reported higher resistance to chloramphenicol and gentamicin, and lower resistance to nalidixic acid as compared to the broth breakpoint method. These results suggest methodology is a critical consideration in the detection and surveillance of antimicrobial resistance phenotypes in Salmonella isolates from poultry samples and could affect the accuracy of population or industry surveillance insights and intervention strategies. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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17 pages, 1254 KiB

Open AccessArticle

Comparison of Quantification Methods to Estimate Farm-Level Usage of Antimicrobials Other than in Medicated Feed in Dairy Farms from Québec, Canada

by Hélène Lardé, David Francoz, Jean-Philippe Roy, Jonathan Massé, Marie Archambault, Marie-Ève Paradis and Simon Dufour

Microorganisms 2021, 9(5), 1106; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9051106 - 20 May 2021

Cited by 11 | Viewed by 2751

Abstract

The objective of the study was to compare three quantification methods to a “garbage can audit” (reference method, REF) for monitoring antimicrobial usage (AMU) from products other than medicated feed over one year in 101 Québec dairy farms. Data were collected from veterinary invoices (VET method), from the “Amélioration de la Santé Animale au Québec” provincial program (GOV method), and from farm treatment records (FARM method). The AMU rate was reported in a number of Canadian Defined Course Doses for cattle (DCDbovCA) per 100 cow-years. Electronic veterinary sales data were obtained for all farms for VET and GOV methods. For the FARM method, a herd management software was used by 68% of producers whereas farm treatment records were handwritten for the others; records could not be retrieved in 4% of farms. Overall, agreement was almost perfect between REF and VET methods (concordance correlation coefficient (CCC) = 0.83), but moderate between REF and GOV (CCC = 0.44), and between REF and FARM (CCC = 0.51). Only a fair or slight agreement was obtained between any alternative method of quantification and REF for oral and intrauterine routes. The billing software used by most of Québec’s dairy veterinary practitioners seems promising in terms of surveillance and benchmarking of AMU in the province. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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20 pages, 20596 KiB

Open AccessArticle

Effect of Antimicrobial Treatment on the Dynamics of Ceftiofur Resistance in Enterobacteriaceae from Adult California Dairy Cows

by David B. Sheedy, Emmanuel Okello, Deniece R. Williams, Katie Precht, Elisa Cella, Terry W. Lehenbauer and Sharif S. Aly

Microorganisms 2021, 9(4), 828; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9040828 - 14 Apr 2021

Cited by 4 | Viewed by 2371

Abstract

Dairy farm use of antimicrobial drugs (AMD) is a risk for the selection of antimicrobial resistance (AMR); however, these resistance dynamics are not fully understood. A cohort study on two dairy farms enrolled 96 cows with their fecal samples collected three times weekly, for the first 60 days in milk. Enterobacteriaceae were enumerated by spiral plating samples onto MacConkey agar impregnated with 0, 1, 8, 16 and 30 µg/mL ceftiofur. Negative binomial regression analyzed AMR over time. The continuum of ceftiofur concentrations permitted estimation of the minimum inhibitory concentration (MIC) and analysis using interval regression. The most common systemic AMD was ceftiofur, administered in 94% of treatments (15/16 cows). Enterobacteriaceae did not grow in 88% of samples collected from non-AMD treated cows at 8 µg/mL ceftiofur. Samples from AMD treated cows had peak counts of resistant Enterobacteriaceae during AMD treatment and returned to baseline counts by 3–4 days post-treatment at 8 µg/mL. Sensitive Enterobacteriaceae (0–1 µg/mL ceftiofur) were reduced below pre-treated levels for 29–35 days post-AMD treatment. Population MIC peaked during AMD treatment and returned to baseline levels by 7–8 days. We conclude that the effect of systemic ceftiofur on the resistance of Enterobacteriaceae in early lactation dairy cows was limited in duration. Full article

(This article belongs to the Special Issue Antimicrobial Stewardship in Food-Producing Animals)

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