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Antibiotic Resistance in Enterobacteriaceae Isolated from Wild Birds
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Sciences, Infectious Diseases.
2011 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The presence and spread of clinically important antibiotic-resistant bacteria in reservoirs from natural environments are not well studied compared to the clinical environments. The overall aim of this project was to study the presence of clinically important antibiotic-resistant bacteria in a reservoir from natural environments. Wild birds were chosen not only as indicators of the level of antibiotic resistance in surrounding natural bacterial populations, but also since birds can act as vectors of several potential pathogens including enteropathogens and because they by migration have an ability to spread these pathogens across geographical regions.

The studies in this thesis showed that wild birds carry antibiotic-resistant enterobacteriaceae. The levels and spectrum of antibiotic resistance varies between different bird populations and geographical regions. In bird populations without interaction with human activities throughout the year, antibiotic resistance is lacking. Antibiotic-resistant bacteria could however probably be dispersed to remote regions by bird migration. Extended-spectrum beta-lactamases (ESBLs) and especially CTX-M types are found in comparable high levels in gull populations considering the recent emergence of these resistance genes in clinical settings. The CTX-M types found in wild birds are the same types that are found in clinical settings and in food producing animals from the same regions. ESBL-producing E. coli isolated from Yellow-legged Gulls are genetically heterogenous, reflecting that these resistance genes are present across the full E. coli genetic diversity. In wild birds CTX-M are found both in E. coli strains with previously known “human signature” as well as “novel” strains. This indicates that these genes are indeed very mobile and rapidly dispersing both through horizontal gene transfer and through successful clones. The findings in this thesis indicate that bird colonies could act as melting pots and reservoirs for new resistance types and that wild birds could act as important indicators of the level of antibiotic resistance dispersal in natural environments.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis , 2011. , 61 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 641
National Category
Medical and Health Sciences
Identifiers
URN: urn:nbn:se:uu:diva-145480ISBN: 978-91-554-8000-4OAI: oai:DiVA.org:uu-145480DiVA: diva2:396256
Public defence
2011-03-25, Hjärnan, Hus 15, Länssjukhuset, Lasarettsvägen, Kalmar, 09:00 (Swedish)
Opponent
Supervisors
Available from: 2011-03-04 Created: 2011-02-09 Last updated: 2012-03-13Bibliographically approved
List of papers
1. Antibiotic susceptibility of faecal bacteria in Antarctic penguins
Open this publication in new window or tab >>Antibiotic susceptibility of faecal bacteria in Antarctic penguins
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2008 (English)In: Polar Biology, ISSN 0722-4060, E-ISSN 1432-2056, Vol. 31, no 6, 759-763 p.Article in journal (Refereed) Published
Abstract [en]

Faecal bacteria from 49 Gentoo penguins on the Antarctic Peninsula were identified by biochemical methods and sequencing, and tested for antibiotic susceptibility using agar dilution. Of the 42 Enterobacteriaceae isolates found, 39 belonged to the genus Edwardsiella. All isolates were susceptible to the 17 antibiotics tested. This implies that antibiotic selection pressure is a prerequisite to a high prevalence of antibiotic resistance, and in the absence of contact with human activities, antibiotic resistance in Enterobacteriaceae remains undetectable.

Keyword
Enterobacteriaceae, Antimicrobial resistance, Edwardsiella, Antarctic Peninsula, Pygoscelis papua, Animal
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-130384 (URN)10.1007/s00300-008-0430-3 (DOI)000255059200013 ()
Available from: 2010-09-07 Created: 2010-09-07 Last updated: 2011-05-04Bibliographically approved
2. Dissemination of multidrug-resistant bacteria into the Arctic
Open this publication in new window or tab >>Dissemination of multidrug-resistant bacteria into the Arctic
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2008 (English)In: Emerging Infectious Diseases, ISSN 1080-6040, E-ISSN 1080-6059, Vol. 14, no 1, 70-72 p.Article in journal (Refereed) Published
Abstract [en]

We show that Escherichia coli isolates originating from Arctic birds carry antimicrobial drug resistance determinants. This finding implies that dissemination of drug-resistant bacteria is worldwide. Resistance genes can be found even in a region where no selection pressure for resistance development exists.

Keyword
Escherichia coli, Arctic birds, Resistance
National Category
Infectious Medicine
Identifiers
urn:nbn:se:uu:diva-88466 (URN)10.3201/eid1401.070704 (DOI)000252142000013 ()18258081 (PubMedID)
Available from: 2009-02-19 Created: 2009-02-02 Last updated: 2011-05-04Bibliographically approved
3. Dissemination of Escherichia coli with CTX-M type ESBL between humans and yellow-legged gulls in the south of France
Open this publication in new window or tab >>Dissemination of Escherichia coli with CTX-M type ESBL between humans and yellow-legged gulls in the south of France
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2009 (English)In: PloS one, ISSN 1932-6203, Vol. 4, no 6, e5958- p.Article in journal (Refereed) Published
Abstract [en]

Extended Spectrum beta-Lactamase (ESBL) producing Enterobacteriaceae started to appear in the 1980s, and have since emerged as some of the most significant hospital-acquired infections with Escherichia coli and Klebsiella being main players. More than 100 different ESBL types have been described, the most widespread being the CTX-M beta-lactamase enzymes (bla(CTX-M) genes). This study focuses on the zoonotic dissemination of ESBL bacteria, mainly CTX-M type, in the southern coastal region of France. We found that the level of general antibiotic resistance in single randomly selected E. coli isolates from wild Yellow-legged Gulls in France was high. Nearly half the isolates (47.1%) carried resistance to one or more antibiotics (in a panel of six antibiotics), and resistance to tetracycline, ampicillin and streptomycin was most widespread. In an ESBL selective screen, 9.4% of the gulls carried ESBL producing bacteria and notably, 6% of the gulls carried bacteria harboring CTX-M-1 group of ESBL enzymes, a recently introduced and yet the most common clinical CTX-M group in France. Multi locus sequence type and phylogenetic group designations were established for the ESBL isolates, revealing that birds and humans share E. coli populations. Several ESBL producing E. coli isolated from birds were identical to or clustered with isolates with human origin. Hence, wild birds pick up E. coli of human origin, and with human resistance traits, and may accordingly also act as an environmental reservoir and melting pot of bacterial resistance with a potential to re-infect human populations.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-113815 (URN)10.1371/journal.pone.0005958 (DOI)000267079500008 ()19536298 (PubMedID)
Available from: 2010-02-04 Created: 2010-02-04 Last updated: 2011-05-04Bibliographically approved
4. Characterization, and comparison, of human clinical and black-headed gull (Larus ridibundus) extended-spectrum β-lactamase-producing bacterial isolates from Kalmar, on the southeast coast of Sweden
Open this publication in new window or tab >>Characterization, and comparison, of human clinical and black-headed gull (Larus ridibundus) extended-spectrum β-lactamase-producing bacterial isolates from Kalmar, on the southeast coast of Sweden
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2010 (English)In: Journal of Antimicrobial Chemotherapy, ISSN 0305-7453, E-ISSN 1460-2091, Vol. 65, no 9, 1939-1944 p.Article in journal (Refereed) Published
Abstract [en]

Antibiotic resistance is one of the great challenges for modern healthcare. In Gram-negative bacteria, CTX-M-type extended-spectrum beta-lactamases (ESBLs) have been rapidly spreading through Europe since the early 2000s. In Sweden, ESBL-producing Escherichia coli are still rare, but a 3-fold increase has been seen from 2004 to 2007. Enterobacteria and normal flora of wild animals, with or without antibiotic resistance traits, constitute a potential source of human infection and colonization. We studied wild birds with the aim to understand the environmental dissemination of antibiotic resistance and, focusing on clinically relevant resistance types, we made comparisons with human clinical samples. In this study, ESBL-producing human clinical isolates and isolates from juvenile black-headed gulls from Kalmar County hospital and the city of Kalmar, respectively, on the southeast coast of Sweden, were characterized and compared. Despite a low frequency of antibiotic resistance among the isolates from gulls, ESBL-producing E. coli isolates were found, two with bla(CTX-M-14) and one with bla(CTX-M-15). The same CTX-M types were dominant among human ESBL isolates. In addition, gull isolates were dispersed among the human samples in the PhenePlate (TM) clustering system, indicating that they neither differ from the human isolates nor form any separate clonal clustering. The finding of CTX-M-type ESBLs in E. coli isolated from black-headed gulls in Sweden, where 'background resistance' is low, is consistent with an ongoing environmental spread of these plasmid-borne resistance genes. The results indicate that a potential for transfer between the human population and environment exists even in countries with a low level of antibiotic resistance.

Keyword
ESBL, CTX-M, clinical, environmental, wild birds
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-135394 (URN)10.1093/jac/dkq222 (DOI)000280921400013 ()
Available from: 2010-12-07 Created: 2010-12-06 Last updated: 2011-05-04Bibliographically approved
5. Globally disseminated human pathogenic Escherichia coli of O25b-ST131 clone, harbouring blaCTX-M-15, found in Glaucous-winged gull at remote Commander Islands, Russia
Open this publication in new window or tab >>Globally disseminated human pathogenic Escherichia coli of O25b-ST131 clone, harbouring blaCTX-M-15, found in Glaucous-winged gull at remote Commander Islands, Russia
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2010 (English)In: Environmental Microbiology Reports, ISSN 1758-2229, Vol. 2, no 2, 329-332 p.Article in journal (Refereed) Published
Abstract [en]

With focus on environmental dissemination of antibiotic resistance among clinically relevant bacteria, such as the rising ESBL type of resistance among Escherichia coli, we investigated antibiotic resistance levels in wild birds in the Commander Islands and Kamchatka, Russia. Despite overall low resistance levels in randomly selected E. coli (one from each sample), we found multi-resistant ESBL-producing E. coli harbouring bla(CTX-M-14) and bla(CTX-M-15) using selective screening. Among these multi-resistant ESBL-producing E. coli we found one bla(CTX-M-15) harbouring strain belonging to the O25b-ST131 clone, recognized for its clonal disseminated worldwide as a human pathogen. The potential in acquiring resistant bacteria of human origin, especially highly pathogenic clones, as well as downstream consequences of that, should not be underestimated but further investigated.

National Category
Medical and Health Sciences Biological Sciences
Identifiers
urn:nbn:se:uu:diva-136037 (URN)10.1111/j.1758-2229.2010.00142.x (DOI)000279432000014 ()
Available from: 2010-12-09 Created: 2010-12-09 Last updated: 2015-01-22Bibliographically approved
6. Antimicrobial susceptibility in Escherichia coli of human and avian origin: a comparison of wild-type distributions
Open this publication in new window or tab >>Antimicrobial susceptibility in Escherichia coli of human and avian origin: a comparison of wild-type distributions
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2009 (English)In: Clinical Microbiology and Infection, ISSN 1198-743X, E-ISSN 1469-0691, Vol. 15, no 5, 461-465 p.Article in journal (Refereed) Published
Abstract [en]

In the present study, the antimicrobial susceptibilities of 97 Escherichia coli isolates from birds, and 100 clinical isolates from blood cultures, were determined by disk diffusion. The wild-type distributions were defined by the normalized resistance interpretation method. It is shown that the avian and clinical inhibition zone diameter distributions of wild-type E. coli are indistinguishable.

Keyword
Antimicrobial susceptibility testing, Escherichia coli, wild-type distributions
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-113810 (URN)10.1111/j.1469-0691.2009.02705.x (DOI)000266110500011 ()19260874 (PubMedID)
Available from: 2010-02-04 Created: 2010-02-04 Last updated: 2011-05-04Bibliographically approved

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