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The effect of tylosin on antimicrobial resistance in beef cattle enteric bacteria: A systematic review and meta-analysis.

ABSTRACT: BACKGROUND:Tylosin is a commonly used in-feed antimicrobial and is approved in several countries to reduce the incidence of liver abscesses in beef cattle. Macrolides are critically important antimicrobials in human health and used to treat some foodborne bacterial diseases, such as Campylobacter jejuni and Salmonella. Feeding tylosin could select for resistant enteric bacteria in cattle, which could contaminate beef products at slaughter and potentially cause foodborne illness. We conducted a systematic review and meta-analysis to evaluate the impact of feeding tylosin to cattle on phenotypic and genotypic resistance in several potential zoonotic enteric bacteria: Enterococcus species, Escherichia coli, Salmonella enterica subspecies enterica, and Campylobacter species. This review was registered with PROSPERO (#CRD42018085949). RESULTS:Eleven databases were searched for primary research studies that fed tylosin at approved doses to feedlot cattle and tested bacteria of interest for phenotypic or genotypic resistance. We screened 1,626 citations and identified 13 studies that met the inclusion criteria. Enterococcus species were tested in seven studies, Escherichia coli was isolated in five studies, three studies reported on Salmonella, and two studies reported on Campylobacter species. Most studies relied on phenotypic antimicrobial susceptibility testing and seven also reported resistance gene testing. A random-effects meta-analyses of erythromycin-resistant enterococci from four studies had significant residual heterogeneity. Only two studies were available for a meta-analysis of tylosin-resistant enterococci. A semi-quantitative analysis demonstrated an increase in macrolide-resistant enterococci after long durations of tylosin administration (>100 days). Semi-quantitative analyses of other bacteria-antimicrobial combinations revealed mixed results, but many comparisons found no effect of tylosin administration. However, about half of these no-effect comparisons did not record the cumulative days of tylosin administration or the time since the last dose. CONCLUSIONS:When fed at approved dosages for typical durations, tylosin increases the proportion of macrolide-resistant enterococci in the cattle gastrointestinal tract, which could pose a zoonotic risk to human beef consumers. Feeding tylosin for short durations may mitigate the impact on macrolide-resistant enterococci and further studies are encouraged to determine the effect of minimizing or eliminating tylosin use in beef cattle. There may also be an impact on other bacteria and other antimicrobial resistances but additional details or data are needed to strengthen these comparisons. We encourage authors of antimicrobial-resistance studies to follow reporting guidelines and publish details of all comparisons to strengthen future meta-analyses.

SUBMITTER: Cazer CL

PROVIDER: S-EPMC7197392 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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The effect of tylosin on antimicrobial resistance in beef cattle enteric bacteria: A systematic review and meta-analysis.

Cazer Casey L CL Eldermire Erin R B ERB Lhermie Guillaume G Murray Sarah A SA Scott H Morgan HM Gröhn Yrjö T YT

Preventive veterinary medicine 20200218

<h4>Background</h4>Tylosin is a commonly used in-feed antimicrobial and is approved in several countries to reduce the incidence of liver abscesses in beef cattle. Macrolides are critically important antimicrobials in human health and used to treat some foodborne bacterial diseases, such as Campylobacter jejuni and Salmonella. Feeding tylosin could select for resistant enteric bacteria in cattle, which could contaminate beef products at slaughter and potentially cause foodborne illness. We condu ...[more]

PMID: 32109782

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Project description:BackgroundWild birds using livestock facilities for food and shelter may contribute to dissemination of enteric pathogens or antimicrobial resistant bacteria. However, drivers of microbial exchange among wildlife and livestock are not well characterized. Predisposition for acquiring and retaining environmental bacteria may vary among species because of physiologic or behavioral differences, complicating selection of a bacterial model that can accurately characterize microbial connections among hosts of interest. This study compares the prevalence and antibiotic resistance phenotypes of two potential model bacterial organisms isolated from wild birds and their environments.MethodsWe compared prevalence and resistance profiles of Escherichia coli and Enterococcus species isolated from environmental swabs and bird feces on a residential control site, a confinement dairy, a pasture-based beef farm, and a confinement beef farm.ResultsBird feces at all sites had low-to-moderate prevalence of Escherichia coli (range: 17-47%), despite potential for exposure on farms (range: 63-97%). Few Escherichia coli were isolated from the control environment. Enterococcus faecalis was dominant in birds at both beef farms (62% and 81% of Enterococcus isolates) and low-to-moderately prevalent at the dairy and control sites (29% and 23% of isolates, respectively). Antimicrobial resistance prevalence was higher in farm samples compared to those from the residential control, but distribution of resistant isolates varied between the bacterial genera. Birds on all farms carried resistant Enterococcus at similar rates to that of the environment, but resistance was less common in bird-associated Escherichia coli despite presence of resistant isolates in the farm environment.DiscussionBacterial species studied may affect how readily bacterial exchange among populations is detected. Selection of microbial models must carefully consider both the questions being posed and how findings might influence resulting management decisions.

Project description:BackgroundAntimicrobial growth promoters (AGPs) are antimicrobial agents administered to livestock in feed for prolonged periods to enhance feed efficiency. Beef cattle are primarily finished in confined feeding operations in Canada and the USA, and the administration of AGPs such as chlortetracycline and sulfamethazine (Aureo S-700 G) is the standard. The impacts of AGPs on the intestinal microbiota of beef cattle are currently uncertain; it is documented that AGPs administered to beef cattle pass through the rumen and enter the intestine. To ascertain the impacts of Aureo S-700 G on the small and large intestinal microbiota of beef cattle (mucosa-associated and within digesta), terminal restriction fragment length polymorphism (T-RFLP) analysis and quantitative PCR (qPCR) for total bacteria were applied. Beef cattle were maintained in an experimental feedlot (five replicate pens per treatment), and AGP treatment cattle were administered Aureo S-700 G in feed, whereas control cattle were administered no antimicrobials. As the intestinal microbiota of beef cattle has not been extensively examined, clone library analysis was applied to ascertain the primary bacterial constituents of the intestinal microbiota.ResultsComparative T-RFLP and qPCR analysis (n = 122 samples) revealed that bacterial community fingerprints and bacterial load within digesta differed from those associated with mucosa. However, the administration of Aureo S-700 G did not affect bacterial community fingerprints or bacterial load within the small and large intestine relative to control cattle. Analysis of >1500 near full length 16S rDNA clones revealed considerably greater bacterial diversity in the large relative to the small intestine of beef cattle. Mucosa-associated bacterial communities in the jejunum were dominated by Proteobacteria, and differed conspicuously from those in the ileum and large intestine. Although the ileum contained bacterial clones that were common to the jejunum as well as the cecum, Firmicutes clones associated with mucosa dominated in the ileum, cecum, and descending colon. In the descending colon, clone library analysis did not reveal a difference in the richness or diversity of bacterial communities within digesta relative to those associated with mucosa. However, T-RFLP analysis indicated a significant difference in T-RF relative abundance (i.e. difference in relative taxon abundance) between mucosa-associated and digesta communities attributed in part to the differential abundance of Bacteriodes, Alistipes, Oscillibacter, and unclassified Clostridiales.ConclusionsThese data demonstrate that there was no significant difference in the composition of the predominant intestinal bacteria constituents within animals administered Aureo S-700 G and those not administered AGPs after a 28 day withdrawal period.

Project description:The specific antimicrobial resistance (AMR) decreases that can be expected from reducing antimicrobial (AM) use in U.S. beef production have not been defined. To address this data gap, feces were recovered from 36 lots of "raised without antibiotics" (RWA) and 36 lots of "conventional" (CONV) beef cattle. Samples (n = 719) were collected during harvest and distributed over a year. AMR was assessed by (i) the culture of six AM-resistant bacteria (ARB), (ii) quantitative PCR (qPCR) for 10 AMR genes (ARGs), (iii) a qPCR array of 84 ARGs, and (iv) metagenomic sequencing. Generally, AMR levels were similar, but some were higher in CONV beef cattle. The prevalence of third-generation cephalosporin-resistant (3GCr) Escherichia coli was marginally different between production systems (CONV, 47.5%; RWA, 34.8%; P = 0.04), but the seasonal effect (summer, 92.8%; winter, 48.3%; P < 0.01) was greater. Erythromycin-resistant (ERYr) Enterococcus sp. concentrations significantly differed between production systems (CONV, 1.91 log10 CFU/g; RWA, 0.73 log10 CFU/g; P < 0.01). Levels of aadA1, ant(6)-I, blaACI, erm(A), erm(B), erm(C), erm(F), erm(Q), tet(A), tet(B), tet(M), and tet(X) ARGs were higher (P < 0.05) in the CONV system. Aggregate abundances of all 43 ARGs detected by metagenomic sequencing and the aggregate abundances of ARGs in the aminoglycoside, β-lactam, macrolide-lincosamide-streptogramin B (MLS), and tetracycline AM classes did not differ (log2 fold change < 1.0) between CONV and RWA systems. These results suggest that further reductions of AM use in U.S. beef cattle production may not yield significant AMR reductions beyond MLS and tetracycline resistance.IMPORTANCE The majority of antimicrobial (AM) use in the United States is for food-animal production, leading to concerns that typical AM use patterns during "conventional" (CONV) beef cattle production in the United States contribute broadly to antimicrobial resistance (AMR) occurrence. In the present study, levels of AMR were generally similar between CONV and "raised without antibiotics" (RWA) cattle. Only a limited number of modest AMR increases was observed in CONV cattle, primarily involving macrolide-lincosamide-streptogramin B (MLS) and tetracycline resistance. Macrolides (tylosin) and tetracyclines (chlortetracycline) are administered in-feed for relatively long durations to reduce liver abscesses. To ensure judicious AM use, the animal health, economic, and AMR impacts of shorter duration in-feed administration of these AMs should be examined. However, given the modest AMR reductions observed, further reductions of AM use in U.S. beef cattle production may not yield significant AMR reductions beyond MLS and tetracycline resistance.

Dataset Information

The effect of tylosin on antimicrobial resistance in beef cattle enteric bacteria: A systematic review and meta-analysis.

Publications

The effect of tylosin on antimicrobial resistance in beef cattle enteric bacteria: A systematic review and meta-analysis.

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