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Antibiotic Resistance Gone Wild Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine 1617 Antibiotic resistance gone wild A One Health perspective on carriage, selection and transmission of Extended-Spectrum Cephalosporinase- and Carbapenemase-producing Enterobacteriaceae CLARA ATTERBY ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6206 ISBN 978-91-513-0817-3 UPPSALA urn:nbn:se:uu:diva-397218 2019 Dissertation presented at Uppsala University to be publicly examined in Tripple room, Navet ground floor, BMC, Husargatan 3, Uppsala, Friday, 24 January 2020 at 09:00 for the degree of Doctor of Philosophy (Faculty of Medicine). The examination will be conducted in English. Faculty examiner: Professor Nicola Williams (Institute of Infection and Global Health in Liverpool, United Kingdom). Abstract Atterby, C. 2019. Antibiotic resistance gone wild. A One Health perspective on carriage, selection and transmission of Extended-Spectrum Cephalosporinase- and Carbapenemase- producing Enterobacteriaceae. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine 1617. 79 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-0817-3. 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. Keywords: Antibiotic resistance, E. coli, K. pneumoniae, ESBL, AmpC, Carbapenemase, ciprofloxacin resistance, colistin resistance, rural, wildlife, birds, sub-MIC, MSC, Cambodia, environment, epidemiology Clara Atterby, Department of Medical Sciences, Akademiska sjukhuset, Uppsala University, SE-75185 Uppsala, Sweden. © Clara Atterby 2019 ISSN 1651-6206 ISBN 978-91-513-0817-3 urn:nbn:se:uu:diva-397218 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-397218) One World – One Health Main supervisor: Associate professor Josef Järhult, Department of Medical Sciences, Uppsala University, Sweden Co-supervisors: Doctor Stefan Börjesson, Department of Animal Health and Antimicrobial Strategies, National Veterinary Institute, Uppsala and Department of Clinical and Experimental Medicine, Linköping University, Sweden Professor Björn Olsen, Department of Medical Sciences, Uppsala University, Sweden Opponent: Professor Nicola Williams, Institute of Infection and Global Health, University of Liverpool, United Kingdom Examining committee: Associate professor Marie Sjölund, Department of Animal Health and Antimicrobial Strategies, National Veterinary Institute, Sweden Professor Diarmaid Hughes, Department of Medical Biochemistry and Microbiology, Uppsala University, Sweden Professor Anita Hällgren, Department of Clinical and Experimental Medicine, Linköping University, Sweden List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Atterby, C., Börjesson, S., Ny, S., Järhult, J. D., Byfors, S., & Bon- nedahl, J. (2017). ESBL-producing Escherichia coli in Swedish gulls-A case of environmental pollution from humans? PloS One, 12(12). II Hessman, J., Atterby, C., Olsen, B., Järhult, J. (2018). High Preva- lence and Temporal Variation of Extended Spectrum β-Lactamase- Producing Bacteria in Urban Swedish Mallards. Microbial Drug Re- sistance, 24:6, 822-829. III Atterby, C., Ramey, A. M., Hall, G. G., Järhult, J., Börjesson, S., & Bonnedahl, J. (2016). Increased prevalence of antibiotic-resistant E. coli in gulls sampled in Southcentral Alaska is associated with urban environments. Infection Ecology & Epidemiology, 6, 32334. IV Atterby, C., Nykvist. M., Lustig, U., Andersson, D., Järhult, J., Sandegren, L. Spread of resistance plasmids and selection of re- sistant bacteria among Mallards exposed to sub-inhibitory concent- rations of antibiotics in their water environment. Manuscript. V Atterby, C., Osbjer, K., Tepper, V, Rajala, E., Hernandez, J., Seng, S., Holl, D., Bonnedahl, J., Börjesson, S., Magnusson, U., Järhult, J. (2019). Carriage of carbapenemase‐ and extended‐spectrum cepha- losporinase‐producing Escherichia coli and Klebsiella pneumoni- ae in humans and livestock in rural Cambodia; gender and age dif- ferences and detection of blaOXA‐48 in humans. Zoonoses and Public Health, 66: 603– 617. Reprints were made with permission from the respective publishers. Contents Introduction ................................................................................................... 11 Bacteria and antibiotic resistance ............................................................. 11 Escherichia coli and Klebsiella pneumoniae ....................................... 11 Factors that drive the emergence and transmission of resistance .............................................................................................. 12 Plasmids ............................................................................................... 13 β-lactams: mode of action and mechanisms of resistance ................... 14 Colistin: mode of action and resistance mechanisms .......................... 16 Fluoroquinolones: mode of action and resistance mechanisms ........... 17 One Health ................................................................................................ 17 Antibiotic resistance from a One Health perspective .......................... 18 Extended spectrum cephalosporinase- and carbapenemase producing Enterobacteriaceae .............................................................. 18 In humans ........................................................................................ 19 In livestock ...................................................................................... 20 In wildlife ........................................................................................ 21 Antibiotic residue and antibiotic resistant bacteria in nature ............... 22 Selection for antibiotic resistance in nature ......................................... 23 Antibiotic resistance and zoonotic disease in Southeast Asia .................. 23 The situation in Cambodia ................................................................... 24 Aims .............................................................................................................. 26 Methods ......................................................................................................... 27 Study design, sampling methods and ethical permits ............................... 27 Questionnaires (Paper V) .......................................................................... 31 Multiple regression model (Paper V) ....................................................... 32 Method of ESCE/K and CPE/K screening (Paper I-III and V) ................ 32 Sample collection and storage ............................................................. 32 Bacterial culturing and species identification ...................................... 32 Phenotypic and genotyping characterization ....................................... 34 Mallard experiment (Paper IV) ................................................................. 34 Construction of experimental bacterial strains .................................... 34 Experimental setup ............................................................................... 35 Transconjugant screening ...................................................................
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