Critically important antimicrobial resistant Enterobacteriaceae in Irish farm effluent and their removal in integrated constructed wetlands

Prendergast, Deirdre M.; O'doherty, A.; Burgess, Catherine M.; Howe, Nicole; McMahon, Frederick; Murphy, Declan; Leonard, Finola C.; Morris, Dearbháile; Harrington, Caolan; Carty, Aila; Moriarty, John; Gutiérrez, Montserrat

doi:10.1016/j.scitotenv.2021.151269

Cited by 11 publications

(12 citation statements)

References 57 publications

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“…Specifically, the qnrS1 gene, confers low level resistance against fluoroquinolones, making more difficult to treat bacterial pathogens carrying this gene [ 21 , 22 ]. The co-resistance to these antibiotic classes can occur in swine ESBL-positive fecal samples [ 23 , 24 ] and it might be linked to the overuse of fluoroquinolones and macrolides to treat animals in Italy [ 25 , 26 ].…”

Section: Discussionmentioning

confidence: 99%

Whole Genome Sequencing (WGS) Analysis of Virulence and AMR Genes in Extended-Spectrum β-Lactamase (ESBL)-Producing Escherichia coli from Animal and Environmental Samples in Four Italian Swine Farms

2022

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Whole genome sequencing (WGS) is a powerful tool to analyze bacterial genomes rapidly, and can be useful to study and detect AMR genes. We carried out WGS on a group of Escherichia coli (n = 30), sampled from healthy animals and farm environment in four pigsties in northern Italy. Two × 250bp paired end sequencing strategy on Illumina MiSeq™ was used. We performed in silico characterization of E. coli isolates through the web tools provided by the Center for Genomic Epidemiology (cge.cbs.dtu.dk/services/) to study AMR and virulence genes. Bacterial strains were further analyzed to detect phenotypic antimicrobial susceptibility against several antimicrobials. Data obtained from WGS were compared to phenotypic results. All 30 strains were MDR, and they were positive for the genes blaCTX-M and blaTEM as verified by PCR. We observed a good concordance between phenotypic and genomic results. Different AMR determinants were identified (e.g., qnrS, sul, tet). Potential pathogenicity of these strains was also assessed, and virulence genes were detected (e.g., etsC, gad, hlyF, iroN, iss), mostly related to extraintestinal E. coli pathotypes (UPEC/APEC). However, enterotoxin genes, such as astA, ltcA and stb were also identified, indicating a possible hybrid pathogenic nature. Various replicons associated to plasmids, previously recovered in pathogenic bacteria, were identified (e.g., IncN and IncR plasmid), supporting the hypothesis that our strains were pathogenic. Eventually, through WGS it was possible to confirm the phenotypic antibiotic resistance results and to appreciate the virulence side of our ESBL-producing E. coli. These findings highlight the need to monitor commensal E. coli sampled from healthy pigs considering a One Health perspective.

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Section: Discussionmentioning

confidence: 99%

Whole Genome Sequencing (WGS) Analysis of Virulence and AMR Genes in Extended-Spectrum β-Lactamase (ESBL)-Producing Escherichia coli from Animal and Environmental Samples in Four Italian Swine Farms

2022

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“…The bla CTX-M-1 -carrying isolates might come either from farms discharging effluents in the nearby rivers or from seabirds’ droppings. Even though we acknowledge that it is very difficult to trace the origin of a strain, such sources of contamination were hypothesized in other contexts [ 31 , 32 ].…”

Section: Discussionmentioning

confidence: 99%

Prevalence and Characterization of Extended-Spectrum β-Lactamase- and Carbapenemase-Producing Enterobacterales from Tunisian Seafood

et al. 2022

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Aquaculture is a rapidly expanding sector in which it is important to monitor the occurrence of multi-drug resistant (MDR) bacteria. The presence of extended-spectrum β-lactamase (ESBL-) or carbapenemase-producing Enterobacterales is a commonly used indicator of the resistance burden in a given sector. In this study, 641 pieces of farmed fish (sea bream and sea bass), as well as 1075 Mediterranean clams, were analyzed. All ESBL- and carbapenemase-producing Enterobacterales collected were whole-genome sequenced. The proportion of ESBL-producing Enterobacterales was 1.4% in fish and 1.6% in clams, carried by Escherichia coli (n = 23) and Klebsiella pneumoniae (n = 4). The ESBL phenotype was exclusively due to the presence of blaCTX-M genes, the most frequent one being blaCTX-M-15. The blaCTX-M-1 gene was also identified in six E. coli, among which four were carried by IncI1/pST3 plasmids, possibly betraying an animal origin. Carbapenemases were absent in fish but identified in two K. pneumoniae isolates from clams (blaNDM-1 and blaOXA-48). Several sequence types (STs) identified were associated with human MDR clones such as E. coli ST131 and ST617, or K. pneumoniae ST307 and ST147. Our results might indicate that bacteria from hospital or farm effluents can reach the open sea and contaminate seafood and fish that are living or raised nearby. Therefore, monitoring the quality of water discharged to the sea and the presence of MDR bacteria in seafood is mandatory to ensure the quality of fishery products.

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“…The detection of mcr -9, in addition to other ARGs, in the ICW influent in this study is concerning, as on farms where no ICW treatment is available this waste may lead to AMR contamination of surrounding surface or ground waters. However, with regards to ICW treatment, while previous studies have reported on the efficacy of this treatment in the reduction of antibiotics, antimicrobial resistant organisms and genes, some have been found to persist in the final effluents (Chen et al ., 2015; Prendergast et al ., 2022). Although mcr -9 was only detected in the influent in this study, there is potential for these genes to persist following treatment.…”

Section: Discussionmentioning

confidence: 99%

“…All ICW samples discussed in this paper were collected and processed as previously described by Prendergast et al ., (2022), while Hooban et al ., (2021) and Hooban et al ., (2022) outlined the collection and processing of all other wastewater samples, as well as water samples. As outlined, the samples were screened for extended-spectrum beta-lactamase (ESBL) producing Enterobacterales, carbapenemase-producing Enterobacterales and fluoroquinolone resistant Enterobacterales, with primary identification of Enterobacterales carried out using matrix-assisted laser desorption/ionization time of flight (MALDI-TOF) mass spectrometry (Bruker).…”

Section: Methodsmentioning

confidence: 99%

First reported detection of the mobile colistin resistance genes,mcr-8 andmcr-9, in the Irish environment

Cahill

Hooban

Fitzhenry

et al. 2022

Preprint

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The emergence and dissemination of mobile colistin resistance (mcr) genes across the globe poses a significant threat to public health, as colistin remains one of the last line treatment options for multi-drug resistant infections. Environmental samples (157 water and 157 wastewater) were collected in Ireland between 2018 and 2020. Samples collected were assessed for the presence of antimicrobial resistant bacteria using Brilliance ESBL, Brilliance CRE, mSuperCARBA and McConkey agar containing a ciprofloxacin disc. All water and integrated constructed wetland influent and effluent samples were filtered and enriched in buffered peptone water prior to culture, while wastewater samples were cultured directly. Isolates collected were identified via MALDI-TOF, were tested for susceptibility to 16 antimicrobials, including colistin, and subsequently underwent whole genome sequencing. Overall, eightmcrpositive Enterobacterales (onemcr-8 and sevenmcr-9) were recovered from six samples (freshwater (n=2), healthcare facility wastewater (n=2), wastewater treatment plant influent (n=1) and integrated constructed wetland influent (piggery farm waste) (n=1)). While themcr-8 positiveK. pneumoniaedisplayed resistance to colistin, all sevenmcr-9 harbouring Enterobacterales remained susceptible. All isolates demonstrated multi-drug resistance and through whole genome sequencing analysis, were found to harbour a wide variety of antimicrobial resistance genes i.e., 30 ± 4.1 (10-61), including the carbapenemases,blaOXA-48 (n=2) andblaNDM-1 (n=1), which were harboured by three of the isolates. Themcrgenes were located on IncHI2, IncFIIK and IncI1-like plasmids. The findings of this study highlight potential sources and reservoirs ofmcrgenes in the environment and illustrate the need for further research to gain a better understanding of the role the environment plays in the persistence and dissemination of antimicrobial resistance.

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Critically important antimicrobial resistant Enterobacteriaceae in Irish farm effluent and their removal in integrated constructed wetlands

Cited by 11 publications

References 57 publications

Whole Genome Sequencing (WGS) Analysis of Virulence and AMR Genes in Extended-Spectrum β-Lactamase (ESBL)-Producing Escherichia coli from Animal and Environmental Samples in Four Italian Swine Farms

Whole Genome Sequencing (WGS) Analysis of Virulence and AMR Genes in Extended-Spectrum β-Lactamase (ESBL)-Producing Escherichia coli from Animal and Environmental Samples in Four Italian Swine Farms

Prevalence and Characterization of Extended-Spectrum β-Lactamase- and Carbapenemase-Producing Enterobacterales from Tunisian Seafood

First reported detection of the mobile colistin resistance genes,mcr-8 andmcr-9, in the Irish environment

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