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Carbapenemase-Producing Enterobacteriaceae in Wastewater-Associated Aquatic Environments
Örebro University, School of Science and Technology.
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The emergence of carbapenem resistance due to the carbapenem-hydrolyzing enzymes (carbapenemases) in Enterobacteriaceae has led to limited therapeutic options. The increased resistance to these “last-resort” antibiotics is fueled by overuse and misuse of antibiotics in human medicine and agriculture. According to the One-Health concept, the microbiomes of humans, animals and natural environments are interconnected reservoirs of antibiotic resistance genes (ARGs) and changes in one compartment will affect the other compartments. Thus, the environmental waters exposed to the pathogens, ARGs and other contaminants of human origin can play a significant role in the spread of resistance. The study aimed to characterize carbapenemase-producing Enterobacteriaceae (CPE) and ARGs in wastewaters and associated river and lake waters in Örebro, Sweden. The study also analyzed de novo development of resistance in Klebsiella oxytoca during long-term growth in river water and the effect of temperature on the emergence of resistance. OXA-48-producing Escherichia coli (ST131) and VIM-1-producing K.oxytoca (ST172) were repeatedly detected in the wastewaters and associated river, suggesting that these isolates were persistently present in these environments. Furthermore, K. oxytoca ST172 isolated from the river was genetically similar to two isolates previously recovered from patients in a local hospital, which shows the possibility of transmission of CPE from hospital to aquatic environments. A high diversity of ARGs was detected in these environments especially in hospital wastewater where ten different carbapenemase genes were detected. These results emphasized that the effective treatment of wastewaters must be ensured to reduce or eliminate the spread of antibiotic resistance. Increased resistance to meropenem (up to 8-fold) and ceftazidime (>10-fold) was observed in K. oxytoca after exposure to both river and tap water after 600 generations and resistance emerged earlier when the bacteria was grown at the higher temperature. The exposure to contaminants and increased environmental temperature may induce similar changes in the environmental microbiome, generating novel resistant variants at accelerated rates that may pose a significant threat to human health.

Place, publisher, year, edition, pages
Örebro: Örebro University , 2020. , p. 81
Series
Örebro Studies in Life Science ; 16
Keywords [en]
Antibiotic resistance evolution, ESBL, Klebsiella, Multidrug, VIM
National Category
Other Biological Topics
Identifiers
URN: urn:nbn:se:oru:diva-81150ISBN: 978-91-7529-334-9 (print)OAI: oai:DiVA.org:oru-81150DiVA, id: diva2:1423620
Public defence
2020-06-08, Örebro universitet, Forumhuset, Hörsal F, Fakultetsgatan 1, Örebro, 10:00 (Swedish)
Opponent
Supervisors
Available from: 2020-04-15 Created: 2020-04-15 Last updated: 2020-05-13Bibliographically approved
List of papers
1. Carbapenemase-producing Escherichia coli ST38 and Klebsiella oxytoca ST172 are persistent in Swedish wastewaters and associated river
Open this publication in new window or tab >>Carbapenemase-producing Escherichia coli ST38 and Klebsiella oxytoca ST172 are persistent in Swedish wastewaters and associated river
(English)Manuscript (preprint) (Other academic)
National Category
Other Biological Topics
Identifiers
urn:nbn:se:oru:diva-81831 (URN)
Available from: 2020-05-13 Created: 2020-05-13 Last updated: 2020-05-13Bibliographically approved
2. Related carbapenemase-producing Klebsiella isolates detected in both a hospital and associated aquatic environment in Sweden
Open this publication in new window or tab >>Related carbapenemase-producing Klebsiella isolates detected in both a hospital and associated aquatic environment in Sweden
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2018 (English)In: European Journal of Clinical Microbiology and Infectious Diseases, ISSN 0934-9723, E-ISSN 1435-4373, Vol. 37, no 12, p. 2241-2251Article in journal (Refereed) Published
Abstract [en]

Carbapenem antibiotics are one of the last-resort agents against multidrug-resistant (MDR) bacteria. The occurrence of carbapenemase-producing Enterobacteriaceae (CPE) in wastewater and aquatic environments is an indication of MDR bacteria in the community. This study evaluated CPE in aquatic environments and compared them to the local hospital isolates in Sweden. Phenotypic and genotypic analyses of antibiotic resistance of environmental and clinical CPE were performed. The relatedness of the isolates and possible clonal dissemination was evaluated using phylogenetic and phyloproteomic analysis. Klebsiella oxytoca carrying carbapenemase genes (blaVIM-1, blaIMP-29) were isolated from wastewater and the recipient river, while K. oxytoca (blaVIM-1) and Klebsiella pneumoniae (blaVIM-1, blaOXA-48, blaNDM-1, blaKPC-3) were isolated from patients at the local clinics or hospital. The K. oxytoca classified as sequence type 172 (ST172) isolated from the river was genotypically related to two clinical isolates recovered from patients. The similarity between environmental and clinical isolates suggests the dispersion of blaVIM-1 producing K. oxytoca ST172 from hospital to aquatic environment and the likelihood of its presence in the community. This is the first report of CPE in aquatic environments in Sweden; therefore, surveillance of aquatic and hospital environments for CPE in other urban areas is important to determine the major transfer routes in order to formulate strategies to prevent the spread of MDR bacteria.

Place, publisher, year, edition, pages
Springer, 2018
Keywords
Antimicrobial resistance, Carbapenemase-producing Enterobacteriaceae, Extended spectrum beta-lactamase, Klebsiella oxytoca, Klebsiella pneumoniae, Multidrug resistance
National Category
Infectious Medicine Microbiology in the medical area
Identifiers
urn:nbn:se:oru:diva-68676 (URN)10.1007/s10096-018-3365-9 (DOI)000449921100003 ()30171482 (PubMedID)2-s2.0-85053311566 (Scopus ID)
Funder
Swedish Research Council Formas, 219-2014-837
Note

Funding Agency:

Nyckelfonden at Orebro University Hospital 

Available from: 2018-09-03 Created: 2018-09-03 Last updated: 2020-05-13Bibliographically approved
3. Diversity of Antibiotic Resistance Genes in Aquatic Environments Using Culture-Dependent and Independent Methods
Open this publication in new window or tab >>Diversity of Antibiotic Resistance Genes in Aquatic Environments Using Culture-Dependent and Independent Methods
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(English)Manuscript (preprint) (Other academic)
National Category
Other Biological Topics
Identifiers
urn:nbn:se:oru:diva-81832 (URN)
Available from: 2020-05-13 Created: 2020-05-13 Last updated: 2020-05-13Bibliographically approved
4. Prevalence and Diversity of Antibiotic Resistance Genes in Swedish Aquatic Environments Impacted by Household and Hospital Wastewater
Open this publication in new window or tab >>Prevalence and Diversity of Antibiotic Resistance Genes in Swedish Aquatic Environments Impacted by Household and Hospital Wastewater
2019 (English)In: Frontiers in Microbiology, ISSN 1664-302X, E-ISSN 1664-302X, Vol. 10, article id 688Article in journal (Refereed) Published
Abstract [en]

Antibiotic-resistant Enterobacteriaceae and non-lactose fermenting Gram-negative bacteria are a major cause of nosocomial infections. Antibiotic misuse has fueled the worldwide spread of resistant bacteria and the genes responsible for antibiotic resistance (ARGs). There is evidence that ARGs are ubiquitous in non-clinical environments, especially those affected by anthropogenic activity. However, the emergence and primary sources of ARGs in the environment of countries with strict regulations for antibiotics usage are not fully explored. The aim of the present study was to evaluate the repertoire of ARGs of culturable Gram-negative bacteria from directionally connected sites from the hospital to the wastewater treatment plant (WWTP), and downstream aquatic environments in central Sweden. The ARGs were detected from genomic DNA isolated from a population of selectively cultured coliform and Gram-negative bacteria using qPCR. The results show that hospital wastewater was a reservoir of several class B beta-lactamase genes such as bla(IMP)(-1), bla(IMP)(-2), and bla(OXA-23), however, most of these genes were not observed in downstream locations. Moreover, beta-lactamase genes such as bla(OXA-48), bla(CDX-M-8), and bla(SFC-1), bla(VIM-1), and bla(VIM-13) were detected in downstream river water but not in the WWTP. The results indicate that the WWTP and hospital wastewaters were reservoirs of most ARGs and contribute to the diversity of ARGs in associated natural environments. However, this study suggests that other factors may also have minor contributions to the prevalence and diversity of ARGs in natural environments.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2019
Keywords
carbapenemase, urban wastewater, surface water, enterobacteriaceae, VIM-1, extended-spectrum beta-lactamase, antimicrobial resistance gene co-occurrence
National Category
Microbiology
Identifiers
urn:nbn:se:oru:diva-73758 (URN)10.3389/fmicb.2019.00688 (DOI)000463403600001 ()
Funder
Swedish Research Council Formas, 219-2014-837Knowledge Foundation, 20150084
Note

Funding Agencies:

Nyckelfonden at Örebro University Hospital  

Örebro University 

Available from: 2019-04-16 Created: 2019-04-16 Last updated: 2020-05-13Bibliographically approved
5. Environmental Conditions Promote Genetic Changes and Increase Resistance to β-lactam Antibiotics in Klebsiella oxytoca
Open this publication in new window or tab >>Environmental Conditions Promote Genetic Changes and Increase Resistance to β-lactam Antibiotics in Klebsiella oxytoca
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Other Biological Topics
Identifiers
urn:nbn:se:oru:diva-81833 (URN)
Available from: 2020-05-13 Created: 2020-05-13 Last updated: 2020-05-13Bibliographically approved

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