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Antimicrobial Resistance and Production of Extended Spectrum Beta-Lactamases in Enterobacteriaceae from Birds in Bangladesh
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Sciences, Clinical Microbiology and Infectious Medicine. (Björn Olsen)
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The dissemination of members of the Enterobacteriaceae family with extended spectrum beta-lactamases (ESBLs) and metallo-beta-lactamases (MBLs) has become a global concern. ESBLs and MBLs have been reported in humans, domestic animals, wildlife and the environment, and their isolation frequencies are increasing rapidly worldwide.  Most studies have been performed in developed countries and quite few in developing countries, where the antibiotic consumption is often poorly controlled. To explore the environmental contamination of antibiotic resistance in Bangladesh, and of ESBLs and MBLs in particular, fecal samples from poultry and wild birds were studied in this thesis.

Samples were collected from both sick birds (poultry having Escherichia coli infections) and healthy birds (free-range poultry, seagulls and crows) residing in different environmental niches. Samples from patients and fresh/sea water were included, to follow the chain of antibiotic resistance in bacteria from humans to the environment. Information regarding the antibiotic usage in poultry production was also collected. The susceptibility of avian E. coli isolates cultured with and without selective pressure was tested against antibiotics commonly used in human and veterinary medicine in Bangladesh. Special attention was paid to ESBL-producing isolates, which were further characterized genetically.

The results of the studies showed that E. coli isolates from commercial poultry, free-range poultry, gulls and crows were resistant to several classes of antibiotics, and that the level and spectrum of antibiotic resistance varied between different bird populations. There was no NDM-producer found among the birds, but ESBL-producing Enterobacteriaceae could be found in up to 59% of the crows, the birds with the highest carriage rate of multiresistant  Enterobacteriaceae of all bird species studied. The most common ESBL-type was CTX-M-15, which also is the most common in the human population in Bangladesh. Birds also shared clinically important sequence types with humans, including E. coli clone O25b-ST131.

In conclusion, ESBL-producing bacteria with multiresistance are easily spread to wild birds. Their opportunistic feeding behavior at poorly managed hospital waste dumps and nearby water bodies makes them into both reservoirs and active spreaders. The high level of antibiotic resistant and ESBL-producing bacteria in the bird population of Bangladesh is worrying, and there is no easy solution in sight. Nationwide programs are necessary to both improve the management of hospital waste and sewage and the control of the antibiotic usage to prevent further environmental contamination. 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2013. , 75 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 911
Keyword [en]
Antimicrobial Resistance, ESBL, CTX-M, NDM, Poultry, Wild birds, E. coli, Bangladesh, Enterobacteriaceae, Antibiotics
National Category
Microbiology in the medical area
Research subject
Epidemiology; Microbiology; Medical Science
Identifiers
URN: urn:nbn:se:uu:diva-199686ISBN: 978-91-554-8691-4 (print)OAI: oai:DiVA.org:uu-199686DiVA: diva2:620961
Public defence
2013-06-12, Hörsalen, Klinisk mikrobiologi, Dag Hammarskjöldsväg 17 ingång D1, Uppsala, 09:00 (English)
Opponent
Supervisors
Note

Time of defence has been changed to 09:00 am on 2013-05-27

Available from: 2013-05-22 Created: 2013-05-13 Last updated: 2013-08-30
List of papers
1. High Prevalence of Antibiotic Resistance in Pathogenic Escherichia coli from Large- and Small-Scale Poultry Farms in Bangladesh
Open this publication in new window or tab >>High Prevalence of Antibiotic Resistance in Pathogenic Escherichia coli from Large- and Small-Scale Poultry Farms in Bangladesh
Show others...
2011 (English)In: Avian diseases, ISSN 0005-2086, E-ISSN 1938-4351, Vol. 55, no 4, 689-692 p.Article in journal (Refereed) Published
Abstract [en]

Antibiotic resistance in avian bacterial pathogens is a common problem in the Bangladesh poultry industry. The aim of the present study was to provide information on the present status of antibiotic resistance patterns in avian pathogenic Escherichia coli in Bangladesh. Of 279 dead or sick poultry of different ages, 101 pathogenic E. coli strains isolated from broilers and layer hens with colibacillosis infections were screened to determine phenotypic expression of antimicrobial resistance against 13 antibiotics used in both veterinary and human medicine in Bangladesh. Of 101 pathogenic E. coli isolates, more than 55% were resistant to at least one or more of the tested compounds, and 36.6% of the isolates showed multiple-drug-resistant phenotypes. The most common resistances observed were against tetracycline (45.5%), trimethoprim-sulphamethoxazole (26.7%), nalidixic acid (25.7%), ampicillin (25.7%), and streptomycin (20.8%). Resistance to ciprofloxacin (12.9%), chlormaphenicol (8.9%), nitrofurantoin (2%), and gentamicin (2%) was also observed, and none of the isolates were resistant to tigecycline as well as extended spectrum beta-lactamase (ESBL) producers. One isolate was resistant to cefuroxime (1%), cefadroxil (1%), and mecillinam (1%) but was not an ESBL producer. Resistance rates, although significant in Bangladeshi isolates, were found to be lower than those reported for avian isolates from the Republic of Korea and clinical, avian, and environmental isolates from Bangladesh. The high level of antibiotic resistance in avian pathogens from Bangladesh is worrisome and indicates that widespread use of antibiotics as feed additives for growth promotion and disease prevention could have negative implications for human and animal health and the environment.

Keyword
Escherichia coli, pathogenic, colibacillosis, antibiotics, antibiotic resistance
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-167635 (URN)000298539000024 ()
Available from: 2012-02-02 Created: 2012-01-31 Last updated: 2017-12-08Bibliographically approved
2. Antimicrobial Drug-Resistant Escherichia coli in Wild Birds and Free-range Poultry, Bangladesh
Open this publication in new window or tab >>Antimicrobial Drug-Resistant Escherichia coli in Wild Birds and Free-range Poultry, Bangladesh
Show others...
2012 (English)In: Emerging Infectious Diseases, ISSN 1080-6040, E-ISSN 1080-6059, Vol. 18, no 12, 2055-2058 p.Article in journal (Refereed) Published
Abstract [en]

Multidrug resistance was found in 22.7% of Escherichia coli isolates from bird samples in Bangladesh; 30% produced extended-spectrum β-lactamases, including clones of CTX-M genes among wild and domestic birds. Unrestricted use of antimicrobial drugs in feed for domestic birds and the spread of resistance genes to the large bird reservoir in Bangladesh are growing problems.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-189246 (URN)10.3201/eid1812.120513 (DOI)000328172700024 ()23171693 (PubMedID)
Available from: 2012-12-28 Created: 2012-12-28 Last updated: 2017-12-06Bibliographically approved
3. Dissemination of NDM-1
Open this publication in new window or tab >>Dissemination of NDM-1
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2012 (English)In: Lancet. Infectious diseases (Print), ISSN 1473-3099, E-ISSN 1474-4457, Vol. 12, no 2, 99-100 p.Article in journal, Letter (Refereed) Published
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-169320 (URN)10.1016/S1473-3099(11)70333-4 (DOI)000299656000009 ()
Available from: 2012-02-28 Created: 2012-02-28 Last updated: 2017-12-07Bibliographically approved
4. The Gull (Chroicocephalus brunnicephalus) as an Environmental Bioindicator and Reservoir for Antibiotic Resistance on the Coastlines of the Bay of Bengal
Open this publication in new window or tab >>The Gull (Chroicocephalus brunnicephalus) as an Environmental Bioindicator and Reservoir for Antibiotic Resistance on the Coastlines of the Bay of Bengal
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2014 (English)In: Microbial Drug Resistance, ISSN 1076-6294, E-ISSN 1931-8448, Vol. 20, no 5, 466-471 p.Article in journal (Refereed) Published
Abstract [en]

The presence and frequency of multiresistant bacteria in wild birds act as indicators of the environmental contamination of antibiotic resistance. To explore the rate of contamination mediated by Escherichia coli, 150 fecal samples from the brown-headed gull (Chroicocephalus brunnicephalus) and 8 water samples from the Bay of Bengal area were collected, cultured, and tested for antibiotic susceptibility. Special attention was paid to extended-spectrum beta-lactamase (ESBL)-producing isolates, which were further characterized genetically. Antibiotic resistance was found in 42.3% (36/85) of the E. coli isolates and multidrug resistance in 11.8%. Isolates from the area with a higher human activity were more resistant than those from an area with a lower level of activity. Most frequent was resistance to ampicillin (29.4%), followed by trimethoprim-sulfamethoxazole (24.7%) and quinolones (22.4%). Carriage of ESBL-producing E. coli was relatively high (17.3%) in the gulls, whereas no ESBL producers were found in the water. All ESBL-producing E. coli isolates, but one, carried blaCTX-M-15 or blaCTX-M-15-like genes. A blaCTX-M-14-like enzyme was found as an exception. Gulls from two different colonies shared E. coli clones and harbored the clinically relevant sequence types ST10, ST48, and ST131. The high frequency of antibiotic resistance and ESBL production among E. coli isolates from gulls indicates that the environmental contamination of antibiotic resistance has already gone far on the coastlines of the Bay of Bengal. Considering the limited control over the antibiotic consumption and waste from human activities in Bangladesh, there is no easy solution in sight.

Keyword
Brown-headed gull, E. coli, antibiotic resistance, blaCTX-M-15, ESBL.
National Category
Veterinary Science Microbiology in the medical area
Research subject
Infectious Diseases; Medical Science
Identifiers
urn:nbn:se:uu:diva-199626 (URN)10.1089/mdr.2013.0233 (DOI)000342303200014 ()24786256 (PubMedID)
Funder
Formas
Available from: 2013-05-08 Created: 2013-05-08 Last updated: 2017-12-06Bibliographically approved
5. Association between Hospital Waste and the House Crow (Corvus splendens) in the Dissemination of Antibiotic Resistance and the Epidemic Escherichia coli Clone O25b-ST131 in Bangladesh
Open this publication in new window or tab >>Association between Hospital Waste and the House Crow (Corvus splendens) in the Dissemination of Antibiotic Resistance and the Epidemic Escherichia coli Clone O25b-ST131 in Bangladesh
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Multiresistant bacteria constitute a serious health risk. In order to investigate the environmental contamination of antibiotic resistance in areas with poor waste management in Bangladesh, fecal samples from 238 house crows living in the surroundings of two major hospitals were screened for members of the Enterobacteriaceae family with extended spectrum beta-lactamase (ESBL)-production. These were compared with 31 ESBL-producing patient isolates, and the susceptibility of E. coli isolates was tested. Without selective pressure, 65.8% of the E. coli isolates from crows were resistant to one or more of 13 antibiotics, and 39.1% were multiresistant. The highest resistance rates were against tetracycline (52.2%), trimethoprim-sulphamethoxazole (43.5%), nalidixic acid (39.8%) and ampicillin (33.5% ). Fifty-nine percent of the crows were ESBL-carriers, and the isolates harbored CTX-M-1, CTX-M-15, CTX-M-55, CTX-M-79 or CTX-M-14-like genes. Two thirds of these ESBL-producers were multi-drug resistant. The ESBL-producing isolates from patients showed a higher rate of resistance compared with the ESBL-producers from crows. One hundred percent were multi-drug resistant, and most common was resistance to ciprofloxacin (93.3%) and trimethoprim-sulphamethoxazole (60%). The corresponding figures for ESBL-producing crow isolates were 41.3% and 57.3%. The crows and patients shared the epidemic E. coli clone O25b-ST131, which carried CTX-M-15 and CTX-M-14-like enzymes. Dissemination of ESBL-producing Klebsiella pneumoniae was also observed among the crows. In conclusion, the Bangladeshi house crow is the bird with the highest carriage rate of ESBL-producing bacteria observed so far. Their scavenging behavior at poorly managed hospital waste dumps, makes them into both reservoirs and active spreaders of antibiotic resistance into the environment. Nationwide programs are necessary to both improve the management of hospital waste and sewage and the control of the antibiotic usage to prevent further environmental contamination. 

Keyword
House crow, E. coli, antibiotic resistance, blaCTX-M-15, ESBL, O25b-ST131
National Category
Veterinary Science Microbiology in the medical area
Research subject
Epidemiology; Medical Science
Identifiers
urn:nbn:se:uu:diva-199627 (URN)
Funder
Formas
Available from: 2013-05-08 Created: 2013-05-08 Last updated: 2013-05-27

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