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Long-term molecular epidemiology of extended-spectrum β-lactamase producing Escherichia coli in a low-endemic setting
Örebro University, School of Medical Sciences.
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Escherichia coli is a commensal inhabitant in the gastro-intestinal tract of humans and animals but it is also the most common bacterial species causing urinary tract infection, which ranges in severity from distal cystitis to urosepsis and septic shock. During the past decades, the prevalence of antibiotic resistant E. coli has increased worldwide. Extended-spectrum β-lactamases (ESBL) causes resistance to β-lactam antibiotics, the most widely used class of antibiotics. The genes encoding ESBL, bla, are usually carried on conjugative plasmids, which can be transferred between different bacterial lineages and different species. These plasmids frequently also carry resistance genes to additional antibiotic classes, and ESBL-producing E. coli are therefore often multidrug-resistant. The aim of this thesis was to describe the long-term molecular epidemiology of ESBL-producing E. coli in Örebro County during the time when they first started to emerge. In addition, potential transmission to the environment was investigated by performing a comparative analysis on ESBL-producing E. coli isolated from patients and from the aquatic environment in Örebro city. In general, the E. coli population was genetically diverse, but the pandemic lineage ST131, first identified in 2004, appears to have been responsible for the dramatic increase of CTX-M-15-producing E.coli observed during the late 2000s. CTX-M-15 was the most prevalent ESBL-type followed by CTX-M-14 and these genes were mainly found on plasmids belonging to the IncF or IncI1 families. Continuous horizontal transmission of IncI1 ST31 and ST37 plasmids between diverse E. coli lineages have also contributed to the dissemination of blaCTX-M-15 in Örebro County. Extended spectrum β-lactamase-producing E. coli were found to be common in the aquatic environment in Örebro city and E. coli lineages genetically similar to those causing infections in humans were present in environmental waters indicating that transmission of ESBL-producing E. colifrom humans to the aquatic environment likely has occurred.

Place, publisher, year, edition, pages
Örebro: Örebro University , 2020. , p. 91
Series
Örebro Studies in Medicine, ISSN 1652-4063 ; 207
Keywords [en]
Escherichia coli, extended-spectrum β-lactamase, whole genome sequencing, plasmids, hybrid assembly, environment, IncI1, ST131
National Category
Other Basic Medicine
Identifiers
URN: urn:nbn:se:oru:diva-79292ISBN: 978-91-7529-324-0 (print)OAI: oai:DiVA.org:oru-79292DiVA, id: diva2:1387530
Public defence
2020-03-20, Örebro universitet, Campus USÖ, hörsal C1, Södra Grev Rosengatan 32, Örebro, 09:00 (Swedish)
Opponent
Supervisors
Available from: 2020-01-22 Created: 2020-01-22 Last updated: 2020-03-26Bibliographically approved
List of papers
1. Molecular and phenotypic characterization of Escherichia coli and Klebsiella pneumoniae producing extended-spectrum β-lactamases with focus on CTX-M in a low-endemic area in Sweden
Open this publication in new window or tab >>Molecular and phenotypic characterization of Escherichia coli and Klebsiella pneumoniae producing extended-spectrum β-lactamases with focus on CTX-M in a low-endemic area in Sweden
2011 (English)In: Acta Pathologica, Microbiologica et Immunologica Scandinavica (APMIS), ISSN 0903-4641, E-ISSN 1600-0463, Vol. 119, no 4-5, p. 287-295Article in journal (Refereed) Published
Abstract [en]

During the last decade increasing prevalence of extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae has been detected worldwide, mainly due to dissemination of Escherichia coli and Klebsiella pneumoniae producing CTX-M-type ESBLs. CTX-M-15 is the most widespread CTX-M type, and the predominant type in various countries. Dissemination of ESBL-producing organisms is caused not only by horizontal transfer of plasmids, but also by clonal spread of ESBL-producing strains. In this study, the molecular epidemiology of class A ESBL (ESBL(A))-producing E. coli and K. pneumoniae isolated in Örebro County, Sweden, was investigated. Out of 200 ESBL(A) -producing E. coli and K. pneumoniae isolates, collected over a 10-year period, 87% were producing CTX-M, belonging to subgroup CTX-M-1 (64%), CTX-M-9 (34%), or CTX-M-2 (2%). The remaining isolates were producing variants of SHV and TEM. Sequencing of the bla(CTX-M) genes revealed 10 different CTX-M types, with a dominance of CTX-M-15 (E. coli 54%, K. pneumoniae 50%) followed by CTX-M-14 (E. coli 28%, K. pneumoniae 27%). Phenotypic characterization of the CTX-M-producing isolates was performed using the PhenePlate system. Although a few minor clusters of CTX-M-15 and CTX-M-14 producers were identified, the majority of the isolates did not appear to be clonally related.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2011
Keywords
Extended-spectrum beta-lactamase; Escherichia coli; Klebsiella pneumoniae; CTX-M; sequencing
National Category
Immunology in the medical area Microbiology in the medical area
Identifiers
urn:nbn:se:oru:diva-25340 (URN)10.1111/j.1600-0463.2011.02730.x (DOI)000289636600008 ()21492229 (PubMedID)2-s2.0-79954726789 (Scopus ID)
Note

Funding Agency:

Research Committee of Orebro County Council, Sweden 

Available from: 2012-08-27 Created: 2012-08-27 Last updated: 2020-02-26Bibliographically approved
2. Characterization of CTX-M-producing Escherichia coli by repetitive sequence-based PCR and real-time PCR-based replicon typing of CTX-M-15 plasmids
Open this publication in new window or tab >>Characterization of CTX-M-producing Escherichia coli by repetitive sequence-based PCR and real-time PCR-based replicon typing of CTX-M-15 plasmids
2014 (English)In: Acta Pathologica, Microbiologica et Immunologica Scandinavica (APMIS), ISSN 0903-4641, E-ISSN 1600-0463, Vol. 122, no 11, p. 1136-1143Article in journal (Refereed) Published
Abstract [en]

The emergence of extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae is a major global concern. CTX-M is the dominating ESBL type worldwide, and CTX-M-15 is the most widespread CTX-M type. The dissemination of CTX-M appears to be in part due to global spread of the Escherichia coli clone O25b-ST131. However, the gene-encoding CTX-M is mainly located on mobile genetic elements, such as plasmids, that also promote the horizontal dissemination of the CTX-M genes. In this study, 152 CTX-M-producing E. coli isolated in 1999-2008 in Örebro County, Sweden, were typed using a commercial repetitive sequence-based PCR (the DiversiLab system), and the prevalence of ST131 was investigated by pabB PCR. Real-time PCR-based plasmid replicon typing was performed on 82 CTX-M-15-producing E. coli isolates. In general, the CTX-M-producing E. coli population was genetically diverse; however, ST131 was highly prevalent (27%), and the dominating clone in our area. The blaCTX -M-15 gene was mainly located on IncF plasmids (69%), but a relatively high proportion of IncI1 plasmids (29%) were also detected among E. coli with diverse rep-PCR patterns, indicating that horizontal transmission of IncI1 plasmids carrying blaCTX -M-15 may have occurred between different E. coli strains.

Place, publisher, year, edition, pages
Malden, USA: John Wiley & Sons, 2014
Keywords
Escherichia coli, ESBL, ST131, plasmid
National Category
Medical and Health Sciences Microbiology
Research subject
Medicine
Identifiers
urn:nbn:se:oru:diva-35271 (URN)10.1111/apm.12270 (DOI)000344383200011 ()24735173 (PubMedID)2-s2.0-84922019604 (Scopus ID)
Note

Funding Agencies:

Research Committee of the County Council of Örebro 

Nyckelfonden at Örebro University Hospital

Available from: 2014-06-09 Created: 2014-06-09 Last updated: 2020-03-26Bibliographically approved
3. Comparative analysis of blaCTX-M-15-IncI1 plasmids in clinical Escherichia coli isolated during a 5-year period in a low-endemic setting
Open this publication in new window or tab >>Comparative analysis of blaCTX-M-15-IncI1 plasmids in clinical Escherichia coli isolated during a 5-year period in a low-endemic setting
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Other Basic Medicine
Identifiers
urn:nbn:se:oru:diva-80208 (URN)
Available from: 2020-02-26 Created: 2020-02-26 Last updated: 2020-02-26Bibliographically approved
4. Comparative distribution of extended-spectrum beta-lactamase-producing Escherichia coli from urine infections and environmental waters
Open this publication in new window or tab >>Comparative distribution of extended-spectrum beta-lactamase-producing Escherichia coli from urine infections and environmental waters
Show others...
2019 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 14, no 11, article id e0224861Article in journal (Refereed) Published
Abstract [en]

Extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli have been reported in natural environments, and may be released through wastewater. In this study, the genetic relationship between ESBL-producing E. coli collected from patient urine samples (n = 45, both hospitalized patients and out-patients) and from environmental water (n = 82, from five locations), during the same time period, was investigated. Three independent water samples were collected from the municipal wastewater treatment plant, both incoming water and treated effluent water; the receiving river and lake; and a bird sanctuary near the lake, on two different occasions. The water was filtered and cultured on selective chromID ESBL agar plates in order to detect and isolate ESBL-producing E. coli. Illumina whole genome sequencing was performed on all bacterial isolates (n = 127). Phylogenetic group B2 was more common among the clinical isolates than the environmental isolates (44.4% vs. 17.1%, p < 0.01) due to a significantly higher prevalence of sequence type (ST) 131 (33.3% vs. 13.4%, p < 0.01). ST131 was, however, one of the most prevalent STs among the environmental isolates. There was no significant difference in diversity between the clinical isolates (DI 0.872 (0.790-0.953)) and the environmental isolates (DI 0.947 (0.920-0.969)). The distribution of ESBL genes was similar: blaCTX-M-15 dominated, followed by blaCTX-M-14 and blaCTX-M-27 in both the clinical (60.0%, 8.9%, and 6.7%) and the environmental isolates (62.2%, 12.2%, and 8.5%). Core genome multi-locus sequence typing showed that five environmental isolates, from incoming wastewater, treated wastewater, Svartån river and Hjälmaren lake, were indistinguishable or closely related (≤10 allele differences) to clinical isolates. Isolates of ST131, serotype O25:H4 and fimtype H30, from the environment were as closely related to the clinical isolates as the isolates from different patients were. This study confirms that ESBL-producing E. coli are common in the aquatic environment even in low-endemic regions and suggests that wastewater discharge is an important route for the release of ESBL-producing E. coli into the aquatic environment.

Place, publisher, year, edition, pages
PLOS, 2019
National Category
Microbiology
Identifiers
urn:nbn:se:oru:diva-77879 (URN)10.1371/journal.pone.0224861 (DOI)31697734 (PubMedID)
Available from: 2019-11-14 Created: 2019-11-14 Last updated: 2020-02-26Bibliographically approved

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