Association between the use of colistin for short-term treatment of Gram-negative bacterial infections and the emergence of colistin-resistant Enterobacteriaceae in swine from selected swine farms in Thailand

Poolperm, Pariwat; Tangkoskul, Teerawit; Seenama, Chakkrapong; Maknakhon, Naruemon; Thamlikitkul, Visanu

doi:10.1371/journal.pone.0238939

Cited by 18 publications

(22 citation statements)

References 31 publications

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“…Expression of some potentially important genes, such as mcr-1, mcr-9, and mcr-10, was not been detected in the piglet gut following colistin treatment. Previous research reported that short-term treatment with colistin is correlated with the emergence of colistin-resistant Enterobacteriaceae in swine (43). The mcr-1 gene was detected in colistin-resistant S. enterica 4, [5],12:i:-isolate from apparently healthy finishing pigs (44).…”

Section: Discussionmentioning

confidence: 91%

Metagenomic Sequencing Analysis of the Effects of Colistin Sulfate on the Pig Gut Microbiome

Li-wei

Zhang

et al. 2021

Front. Vet. Sci.

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The gut microbiome plays important roles in maintaining host health, and inappropriate use of antibiotics can cause imbalance, which may contribute to serious disease. However, despite its promise, using metagenomic sequencing to explore the effects of colistin on gut microbiome composition in pig has not been reported. Herein, we evaluated the roles of colistin in gut microbiome modulation in pigs. Metagenomic analysis demonstrated that overall microbial diversity was higher in the colistin group compared with the control group. Antibiotic Resistance Genes Database analysis demonstrated that following colistin treatment, expression levels of tsnr, ant6ia, tetq, oleb, norm, ant3ia, and mexh were significantly upregulated, indicating that colistin may induce transformation of antibiotic resistance genes. Colistin also affected the microbiome distribution patterns at both genus and phylum levels. In addition, at the species level, colistin significantly reduced the abundance of Prevotella copri, Phascolarctobacterium succinatutens, and Prevotella stercorea and enhanced the abundance of Treponema succinifaciens and Acidaminococcus fermentans compared to the control group. Gene Ontology analysis demonstrated that following treatment with colistin, metabolic process, cellular process, and single-organism process were the dominant affected terms. Kyoto Encyclopedia of Genes and Genomes analysis showed that oxidative phosphorylation, protein processing in endoplasmic reticulum, various types of N-glycan biosynthesis, protein processing in endoplasmic reticulum, pathogenic Escherichia coli infection, and mitogen-activated protein kinase signaling pathway–yeast were the dominant signaling pathways in the colistin group. Overall, our results suggested that colistin affects microbial diversity and may modulate gut microbiome composition in pig, potentially providing novel strategy or antibiotic rationalization pertinent to human and animal health.

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Section: Discussionmentioning

confidence: 91%

Metagenomic Sequencing Analysis of the Effects of Colistin Sulfate on the Pig Gut Microbiome

Li-wei

Zhang

et al. 2021

Front. Vet. Sci.

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“…2) to a point were weaned piglets were treated more than 60 out of 100 days in October 2016. This is not a sustainable situation from an animal welfare point of view, a financial perspective of the farmer and the perspective of emerging antimicrobial resistance against polymyxins [39][40][41]. Because antimicrobial therapy only reduces shedding once treatment of clinically sick pigs has started, untreated pigs can shed Salmonella, resulting in rapid spread to other compartments and corridors of the farm.…”

Section: Discussionmentioning

confidence: 99%

Salmonella Typhimurium environmental reduction in a farrow-to-finish pig herd using a live attenuated Salmonella Typhimurium vaccine

Wolf¹,

Meijerink²,

Libbrecht³

et al. 2021

Porc Health Manag

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Background Salmonella Typhimurium is an important zoonotic pathogen in pigs, that can cause clinical disease. Many sow herds and finishing herds are infected with Salmonella, and therefore pose a threat for the contamination of pork and pork products and ultimately consumers. Case presentation This case study describes a farrow-to-finish pig herd, producing its own replacement gilts, which had experienced clinical outbreaks of salmonellosis since 2002. Outbreaks were characterised by profuse diarrhoea, dead pigs and high antimicrobial use (colistin sulphate). The aim of this study was to see whether using vaccination of sows and piglets with Salmoporc®, a live attenuated Salmonella Typhimurium vaccine, in combination with standard hygienic precautions, it was possible to reduce Salmonella Typhimurium to below the bacteriological detection limit. Monitoring of the presence of Salmonella was done using a total of 20 pooled faecal, sock and dust samples per herd visit in the period from September 2016 to October 2020. Within the first 10 months after the start of vaccination in August 2016, there was a rapid reduction in clinical symptoms, antimicrobial usage and the number of Salmonella-positive samples. During the winters of 2017/2018 and 2018/2019 the number of positive samples increased again, however with minimal need to use antimicrobials to treat the affected animals. In July 2019, only two samples from a corridor were positive. In September and November 2019 and in October 2020 all three samplings were completely negative for S. Typhimurium. Conclusions This case, together with other longitudinal studies, can be seen as a proof of the principle that long term vaccination with a live attenuated S. Typhimurium vaccine can reduce the level of S. Typhimurium in the herd environment to very low levels within a farrow-to-finish herd initially suffering from clinical salmonellosis. Also, clinical symptoms indicating salmonellosis were no longer observed and antimicrobials to treat clinically diseased pigs were no longer needed.

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“…Some studies (Nguyen et al, 2016;Poolperm et al, 2020) have suggested an association between AMU and colistin resistance of Enterobacterales isolated from food-producing animals in Southeast Asia.…”

Section: Main Findingsmentioning

confidence: 99%

Modelling the impact of antimicrobial use and external introductions on commensal E. coli colistin resistance in small‐scale chicken farms of the Mekong delta of Vietnam

Bastard

Nhung

Hien³

et al. 2022

Transbounding Emerging Dis

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Colistin is a critically important antimicrobial for human medicine, and colistin‐resistant Escherichia coli are commonly found in poultry and poultry products in Southeast Asia. Here, we aim at disentangling the within‐farm and outside‐farm drivers of colistin resistance in small‐scale chicken farms of the Mekong delta of Vietnam. Nineteen Vietnamese chicken farms were followed up along a whole production cycle, during which weekly antimicrobial use data were recorded. At the beginning, middle and end of each production cycle, commensal E. coli samples from birds were collected, pooled and tested for colistin resistance. Twelve models were fitted to the data using an expectation–maximization algorithm and compared. We further tested the spatial clustering of the occurrence of resistance importations from external sources using the local Moran's I statistic. In the best model, colistin resistance in E. coli from chickens was found to be mostly affected by importations of resistance, and, to a lesser extent, by the use of antimicrobials in the last 1.73 weeks [0.00; 2.90], but not by the use of antimicrobials in day‐olds, nor their colistin resistance carriage from hatchery. The occurrence of external source importations proved to be sometimes spatially clustered, suggesting a role of local environmental sources of colistin resistance.

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Association between the use of colistin for short-term treatment of Gram-negative bacterial infections and the emergence of colistin-resistant Enterobacteriaceae in swine from selected swine farms in Thailand

Cited by 18 publications

References 31 publications

Metagenomic Sequencing Analysis of the Effects of Colistin Sulfate on the Pig Gut Microbiome

Metagenomic Sequencing Analysis of the Effects of Colistin Sulfate on the Pig Gut Microbiome

Salmonella Typhimurium environmental reduction in a farrow-to-finish pig herd using a live attenuated Salmonella Typhimurium vaccine

Modelling the impact of antimicrobial use and external introductions on commensal E. coli colistin resistance in small‐scale chicken farms of the Mekong delta of Vietnam

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