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Carriage of carbapenemase- and extended-spectrum cephalosporinase-producing Escherichia coli and Klebsiella pneumoniae in humans and livestock in rural Cambodia: gender and age differences and detection of blaOXA-48 in humans
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Sciences, Infection medicine.ORCID iD: 0000-0001-7360-5383
Swedish Univ Agr Sci SLU, Dept Clin Sci, Div Reprod, Uppsala, Sweden; Food & Agr Org United Nations, Phnom Penh, Cambodia.
Swiss Fed Inst Technol, Inst Environm Engn, Zurich, Switzerland.
Swedish Univ Agr Sci SLU, Dept Clin Sci, Div Reprod, Uppsala, Sweden.
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2019 (English)In: Zoonoses and Public Health, ISSN 1863-1959, E-ISSN 1863-2378, Vol. 66, no 6, p. 603-617Article in journal (Refereed) Published
Abstract [en]

Objectives: This study investigates the frequency and characteristics of carbapenemase‐producing Escherichia coli/Klebsiella pneumoniae (CPE/K) and extended‐spectrum cephalosporinase‐producing E. coli/K. pneumoniae (ESCE/K) in healthy humans and livestock in rural Cambodia. Additionally, household practices as risk factors for faecal carriage of ESCE/K are identified.

Methods: Faecal samples were obtained from 307 humans and 285 livestock including large ruminants, pigs and poultry living in 100 households in rural Cambodia in 2011. Each household was interviewed, and multilevel logistic model determined associations between household practices/meat consumption and faecal carriage of ESCE/K. CPE and ESCE/K were detected and further screened for colistin resistance genes.

Results: CPE/K isolates harbouring blaOXA‐48 were identified in two humans. The community carriage of ESCE/K was 20% in humans and 23% in livestock. The same ESBL genes: blaCTX‐M‐15, blaCTX‐M‐14, blaCTX‐M‐27, blaCTX‐M‐55, blaSHV‐2, blaSHV‐12, blaSHV‐28; AmpC genes: blaCMY‐2, blaCMY‐42, blaDHA‐1; and colistin resistance genes: mcr‐1‐like and mcr‐3‐like were detected in humans and livestock. ESCE/K was frequently detected in women, young children, pigs and poultry, which are groups in close contact. The practice of burning or burying meat waste and not collecting animal manure indoors and outdoors daily were identified as risk factors for faecal carriage of ESCE/K.

Conclusions: Faecal carriage of E. coli and K. pneumoniae harbouring extended‐spectrum cephalosporinase genes are common in the Cambodian community, especially in women and young children. Exposure to animal manure and slaughter products are risk factors for intestinal colonization of ESCE/K in humans.

 

Place, publisher, year, edition, pages
2019. Vol. 66, no 6, p. 603-617
Keywords [en]
AmpC, Cambodia, ESBL, carbapenemase, colistin, risk factors, rural population, zoonoses
National Category
Infectious Medicine
Identifiers
URN: urn:nbn:se:uu:diva-388725DOI: 10.1111/zph.12612ISI: 000473968900001PubMedID: 31264805OAI: oai:DiVA.org:uu-388725DiVA, id: diva2:1335058
Funder
Swedish Civil Contingencies AgencySida - Swedish International Development Cooperation Agency, 2010-7876Swedish Research Council, 2016-02606Available from: 2019-07-03 Created: 2019-07-03 Last updated: 2019-11-20Bibliographically approved
In thesis
1. Antibiotic resistance gone wild: A One Health perspective on carriage, selection and transmission of Extended-Spectrum Cephalosporinase- and Carbapenemase-producing Enterobacteriaceae
Open this publication in new window or tab >>Antibiotic resistance gone wild: A One Health perspective on carriage, selection and transmission of Extended-Spectrum Cephalosporinase- and Carbapenemase-producing Enterobacteriaceae
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Antibiotics have saved millions of lives since they came into clinical use during the Second World War in the 1940s. Today, our effective use of antibiotics is under great threat due to emerging antibiotic resistance in bacteria. This thesis addresses the problems of antibiotic resistance from a ”One Health” perspective. The focus is on antibiotic resistant Escherichia coli (E. coli) and Klebsiella pneumoniae (K. pneumoniae) in the environment and wildlife, and also considering the situation in healthy humans and livestock. 

In Paper I-III, high occurrence of Extended-Spectrum Beta-Lactamase (ESBL) -producing E. coli and/or K. pneumoniae was detected in fecal samples from wild birds, and the bacteria had genetic similarities to bacteria that cause disease in humans. Proximity to humans was associated with higher occurrence of cephalosporinase (ESBL and pAmpC)-producing E. coli in wild gulls. In Paper IV, ciprofloxacin resistant E. coli was enriched in the gut of mallards exposed to low concentrations of ciprofloxacin, and plasmid conjugation between E. coli bacteria readily took place. In Paper V, carbapenem resistant and blaOXA-48 harbouring- E. coli/K. pneumoniae was rare, but present in healthy humans in rural Cambodia, while cephalosporinase-producing E. coli/K. pneumoniae was common in both humans and livestock. The same ESBL/pAmpC genes were detected in humans and livestock, and exposure to animal manure and slaughter products were risk factors for fecal carriage in humans.

In conclusion, wild birds can function as potential resistance reservoirs and sentinels for antibiotic resistant E. coli. Environmental pollution from humans is the primary source for antibiotic resistant Enterobacteriaceae found in wildlife, but selection for antibiotic resistant bacteria may also occur in wild birds. The results indicate that transmission of cephalosporinase-producing E. coli/K. pneumoniae occur between wildlife, humans and livestock, but more in-depth molecular work is needed to determine the mechanisms of dissemination. The high community carriage of multidrug-resistant bacteria in rural Cambodia is worrying and highlights Southeast Asia as a hotspot for antibiotic resistance. Antibiotic resistance surveillance is biased towards high-income countries and research should be focused more on low- and middle-income countries, and also include the important “One Health” perspective.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2019. p. 79
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1617
Keywords
Antibiotic resistance, E. coli, K. pneumoniae, ESBL, AmpC, Carbapenemase, ciprofloxacin resistance, colistin resistance, rural, wildlife, birds, sub-MIC, MSC, Cambodia, environment, epidemiology
National Category
Microbiology in the medical area
Research subject
Infectious Diseases
Identifiers
urn:nbn:se:uu:diva-397218 (URN)978-91-513-0817-3 (ISBN)
Public defence
2020-01-24, Tripple room, Navet ground floor, BMC, Husargatan 3, Uppsala, 09:00 (English)
Opponent
Supervisors
Available from: 2019-12-18 Created: 2019-11-20 Last updated: 2020-01-13

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Atterby, ClaraJärhult, Josef D.

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