Competitive Exclusion Reduces Transmission and Excretion of Extended-Spectrum-β-Lactamase-Producing Escherichia coli in Broilers

Ceccarelli, Daniela; Essen-Zandbergen, Alieda van; Smid, Bregtje; Veldman, Kees; Boender, Gert Jan; Fischer, E.A.J.; Mevius, Dik; Goot, J.A. van der

doi:10.1128/aem.03439-16

Cited by 51 publications

(82 citation statements)

References 45 publications

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“…The threat that ESBL-producing Enterobacteriaceae from poultry pose to public health must be taken into serious consideration when discussing antibiotic resistance in farm animals. Different approaches to reduce the prevalence and spread of these bacteria in poultry by the use of feed additives showed promising results [14][15][16]21]. However, to our best knowledge, their impact on both prevalence and horizontal gene transfer has not been studied in poultry.…”

Section: Discussionmentioning

confidence: 99%

“…It was previously shown in vivo, that DFM can reduce the prevalence of ESBL-producing E. coli in the ceca of broiler chicks [14,15], corresponding with the results from this in vivo trial. Another study investigated the transmission of ESBL-producing E. coli (CTX-M-1) between animals, where animals perceiving the DFMs were less susceptible to ESBL-producing E. coli and excreted lower numbers of these bacteria [16]. The effect observed in these studies were based on competitive exclusion.…”

Section: Discussionmentioning

confidence: 99%

“…The negative impact of DFMs, such as various Lactobacillus strains, on the prevalence of pathogens has been described frequently [12,13]. To our best knowledge, only three studies demonstrating the impact of DFMs and competitive exclusion cultures on prevalence and transfer of ESBL-producing Enterobacteriaceae in broilers have been published [14][15][16]. These studies comprise commercial products and competitive exclusion cultures, however no exact qualitative and quantitative specification of the containing microorganisms was provided.…”

Section: Introductionmentioning

confidence: 99%

“…On the one hand, the transmission between animals and from animals to humans must be considered. Several studies have targeted this topic with one trial specifically covering the transmission of ESBL-producing Enterobacteriaceae between broilers receiving DFM [16]. On the other hand, horizontal gene transfer of ESBL-carrying plasmids must also be considered as antibiotic resistance genes are frequently exchanged between bacteria [22,23].…”

Section: Introductionmentioning

confidence: 99%

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The Impact of Direct-Fed Microbials and Phytogenic Feed Additives on Prevalence and Transfer of Extended-Spectrum Beta-Lactamase Genes in Broiler Chicken

et al. 2020

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Poultry frequently account for the highest prevalence of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in livestock. To investigate the impact of direct-fed microbials (DFM) and phytobiotic feed additives on prevalence and conjugation of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae, an animal trial was conducted. Lactobacillus agilis LA73 and Lactobacillus salivarius LS1 and two commercial phytogenic feed additives (consisting of carvacrol, cinnamaldehyde, and eugenol) were used as feed additives either alone or as a combination of DFM and phytogenic feed additive. An ESBL-producing E. coli donor and a potentially pathogenic Salmonella Typhimurium recipient were inoculated at 5 × 109 cells/mL in cecal contents from 2-week-old broilers. Conjugation frequencies were determined after 4 h aerobic co-incubation at 37 °C and corrected for the impact of the sample matrix on bacterial growth of donor and recipient. Surprisingly, indigenous Enterobacteriaceae acted as recipients instead of the anticipated Salmonella recipient. The observed increase in conjugation frequency was most obvious in the groups fed the combinations of DFM and phytogenic product, but merely up to 0.6 log units. Further, cecal samples were examined for ESBL-producing Enterobacteriaceae on five consecutive days in broilers aged 27–31 days. All samples derived from animals fed the experimental diet showed lower ESBL-prevalence than the control. It is concluded that Lactobacillus spp. and essential oils may help to reduce the prevalence of ESBL-harboring plasmids in broilers, while the effect on horizontal gene transfer is less obvious.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Impact of Direct-Fed Microbials and Phytogenic Feed Additives on Prevalence and Transfer of Extended-Spectrum Beta-Lactamase Genes in Broiler Chicken

et al. 2020

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“…On the other hand, if fitness costs are high enough in vivo, plasmid-carrying bacteria should ultimately disappear by competitive exclusion. Competitive exclusion has earlier been shown effective at decreasing the levels of ESBL-producing E. coli in broilers that received cultures containing several different species (13)(14)(15). The issue then arises of whether this is caused by direct competition between ESBL-producing E. coli populations and ESBL-free E. coli populations.…”

mentioning

confidence: 99%

Competition between Escherichia coli Populations with and without Plasmids Carrying a Gene Encoding Extended-Spectrum Beta-Lactamase in the Broiler Chicken Gut

Fischer

Dierikx

Essen-Zandbergen

et al. 2019

Appl Environ Microbiol

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Extended-spectrum-beta-lactamase (ESBL)/AmpC-producing Escherichia coli strains are widely found in E. coli isolates from broiler feces, largely due to the presence of the blaCTX-M-1 gene on IncI1 plasmids. Plasmid carriage is theorized to cause fitness loss and thus should decrease under conditions of reduced antibiotic use. However, in vitro studies showed plasmid carriage to increase in the absence of antimicrobials, due to plasmid conjugation. We investigated whether this translates to increased levels of plasmid in the gastrointestinal tracts of chickens, where conjugation rates may be different and subtle differences in growth rates may have a larger impact on colonization. Eight groups of five chickens were orally inoculated at 4 days of age with a 0.5-ml volume containing 106 CFU/ml E. coli cells, of which 0%, 0.1%, 10%, or 100% carried the IncI1 plasmid with the gene blaCTX-M-1. At 13 time points during 41 days, fecal samples were taken from each chicken. E. coli strains with and without plasmids were quantified. Trends in E. coli subpopulations were analyzed using generalized linear mixed models, and population dynamics were studied by fitting to a mechanistic model. Trends in E. coli subpopulations were different between groups rather than between individual chickens, suggesting substantial levels of E. coli exchange between chickens in a group. The IncI1 plasmid carrying blaCTX-M-1 was transferred with conjugation coefficients at levels higher than those observed in vitro. Across groups, the plasmids disappeared or were established independently of the initial fraction of plasmid-carrying E. coli, but no major increase occurred as observed in vitro. Differences in growth rates were observed, but competitive exclusion of plasmid-carrying variants was counteracted by conjugation. IMPORTANCE Bacteria that produce extended-spectrum beta-lactamases are resistant to an important class of antimicrobials in human and veterinary medicine. Reduction in antibiotic use is expected to decrease the prevalence of resistance. However, resistance genes often lie on plasmids which can be copied and transferred to other bacteria by conjugation, so in vitro resistance was observed to increase in the absence of antimicrobials. We sought to determine whether this also occurs in the chicken gut and if competitive exclusion by similar E. coli variants without the resistance occurred. We studied the excretion of E. coli carrying IncI1 plasmids with the blaCTX-M-1 resistance gene in small groups of broiler chickens, after inoculating the chickens with E. coli suspensions containing different fractions of plasmid-carrying cells. Our results showed little variation between chickens within groups but large differences between groups that were independent of the ratio of variants with and without the plasmid and with persistence or extinction of the plasmid. However, there was no major plasmid increase as observed in vitro. We conclude that in vivo studies with sufficient independent replications are important for intervention studies on plasmid-mediated antimicrobial resistance.

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Gastrointestinal Tract Barrier Efficiency: Function and Threats

Yakout¹,

Eckhardt²

2022

Gut Microbiota, Immunity, and Health in Production Animals

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Competitive Exclusion Reduces Transmission and Excretion of Extended-Spectrum-β-Lactamase-Producing Escherichia coli in Broilers

Cited by 51 publications

References 45 publications

The Impact of Direct-Fed Microbials and Phytogenic Feed Additives on Prevalence and Transfer of Extended-Spectrum Beta-Lactamase Genes in Broiler Chicken

The Impact of Direct-Fed Microbials and Phytogenic Feed Additives on Prevalence and Transfer of Extended-Spectrum Beta-Lactamase Genes in Broiler Chicken

Competition between Escherichia coli Populations with and without Plasmids Carrying a Gene Encoding Extended-Spectrum Beta-Lactamase in the Broiler Chicken Gut

Gastrointestinal Tract Barrier Efficiency: Function and Threats

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