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Phenotypic and Molecular Characterisation of Pseudomonas Aeruginosa Infections from Companion Animals and Potential Reservoirs of Antibacterial Resistance in Humans

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Phenotypic and Molecular Characterisation of Pseudomonas Aeruginosa Infections from Companion Animals and Potential Reservoirs of Antibacterial Resistance in Humans Phenotypic and molecular characterisation of Pseudomonas aeruginosa infections from companion animals and potential reservoirs of antibacterial resistance in humans. Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Master of Philosophy by Andrea Catherine Scott May 2018 Acknowledgements I would like to thank my primary supervisors Dr Joanne Fothergill and Dr Alan Radford. I also thank my secondary supervisors Dr Dorina Timofte, Dr Vanessa Schmidt, Dr Gina Pinschbeck and Dr Neil McEwan and the Institute of Infection and Global Health, University of Liverpool and Professor Craig Winstanley, along with the Small Animal Teaching Hospital (SATH), Leahurst, University of Liverpool and the Veterinary Diagnostic Laboratory (VDL), Leahurst. Matthew Moore (PhD student at University of Liverpool) performed Bioinformatics work for this project. The sequencing in this project was performed as part of the International Pseudomonas Consortium. The Masters thesis of this work was supported through a University of Liverpool/Wellcome Trust Research taster fellowship and internal funding. 2 Abbreviations AMR – Antimicrobial resistance BSAVA – British Small Animal Veterinary Association BVA – British Veterinary Association CDC - Centre for Disease Control and Prevention CF – Cystic fibrosis COPD – Chronic obstructive pulmonary disorder CRE – Carbepenam-resistant enterobacteriacea ECDPC - European Centre Disease Prevention and Control FDA – US Food and Drug Administration HAIs – Hospital acquired infections ICEs – Integrative and conjugative elements ICUs – Intensive care units IDSA - Infectious Diseases Society of America LPS – Lipopolysaccharide LES –Liverpool epidemic strain MDR - Multi drug resistant MMR – Mis-match repair genes MRSA - Methicillin-resistant Staphylococcus aureus OM - Outer membrane PCR – Polymerase chain reaction PFGE – Pulse-field gel electrophoresis PHE – Public Health England VAP – Ventilator associated pneumonia VMTH – Veterinary Medicine Teaching Hospital WHO - World Health Organisation WGS – Whole genome sequencing 3 Abstract........................................................................................................................6 Chapter1: Introduction.……………......................................................................................8 1.1 Pseudomonas aeruginosa..........................................................................................8 1.2 P.aeruginosa infections in humans….......................................................................13 1.3 Circulating P.aeruginosa strain types in humans and diversity of the population structure ……………………..…………………………………………………………………........................18 1.4 Limited antimicrobial treatment options in treatment of P.aeruginosa infections in humans.……………………………………..…..........................................................................23 1.5 P.aeruginosa infections in animals..........................................................................26 1.6 Antimicrobial treatments used for P.aeruginosa infections in animals................30 1.7 AMR in P.aeruginosa.……………………….………………………..……………………………...……34 1.8 Potential for cross-species transmission between humans and animals.............35 Chapter 2: Materials and Methods for Results Chapter 3 - Reservoirs of resistance: polymyxin resistance in veterinary-associated isolates of P. aeruginosa……………….41 2.1 Bacterial isolates…..……............................................................................................41 2.2 Susceptibility testing.…..……………….........................................................................43 2.3 Clondiag Array Tube.……….………………………………………….......................................44 2.4 Genomic DNA extraction for Illumina sequencing...……………………….…………….….50 2.5 Whole Genome Sequencing (Illumina) of Bacterial Isolates ……………………………52 2.6 Genomics .……………………………………………………………………………………………………….53 2.7 Comprehensive Antibiotic Resistance Database sequence data analysis …………54 2.8 eBurst algorithm ……...…………………………….……………………..……………………………….55 2.9 Statistical Analysis……………………………………………………………………….……………….….56 Chapter 2: Materials and Methods for Results Chapter 4 - PCR characterisation of antibiotic resistant determinants in P. aeruginosa from companion animals………..57 2.10 Bacterial isolates …………………………….................................................................57 2.11 Susceptibility testing …..…………………………….……………........................................60 2.12 DNA Extraction………..........................................................................................62 2.13 Polymerase Chain Reactions ……………………………………………………………….……....63 2.14 Primers ..……………………………………………………………………….…………………….……….66 2.15 Quantification and purity testing of genomic DNA by NanoDrop spectrophotometer……………………………………………………………………………………………….66 4 2.16 DNA Sequencing ..……...………………………………………………….………..……………………67 2.17 Statistics ……………………………………………………………………………………………………….67 Chapter 3: Reservoirs of resistance: polymyxin resistance in veterinary-associated isolates of Pseudomonas aeruginosa .…….……….……..................................................68 3.1 Introduction.……………….…………………….……………..................................................68 3.2 Aims.………………….…………………………………………………….........................................76 3.3 Results .……………………….……………………………........................................................77 3.4 Discussion .…………………………………………………………..............................................90 3.5 Conclusions.……………….……………………….……….....................................................98 Chapter 4: PCR characterisation of antibiotic resistant determinants in P. aeruginosa from companion animals..…………………………………………,…….……………….….................99 4.1 Introduction.……….…………………………………………………..........................................99 4.2 Aims.……………………….……………………………….………….…………….............................128 4.3 Results .……………………….……………………………………….…….....................................129 4.4 Discussion.………………………………………………………………..…….……..........................165 4.5 Conclusions.……………….……………………………………….……………..............................170 Chapter 5: Discussion..…………………………………………………………………………………………171 References ..…………………………………………………………………………………………………….….182 5 Phenotypic and molecular characterisation of Pseudomonas aeruginosa infections from companion animals and potential reservoirs of antibacterial resistance in humans. Andrea Catherine Scott - May 2018 Abstract Antimicrobial resistance (AMR) is a multifactorial and complex issue, affecting healthcare worldwide. This is an escalating concern, highlighted by European and International bodies. AMR is not only a concern in human health but also animal health. The close interface between people, pets, food production animals and the environment exemplifies the importance that these two areas of health should not be considered as independent factions. Pseudomonas aeruginosa is a formidable pathogen due to its innate resistance making it naturally insensitive to many classes of antimicrobials, alongside its ability to acquire further resistance mechanisms. P. aeruginosa in the veterinary setting is a clinically relevant pathogen often associated with disease. In this project, I determined the susceptibility of a set of veterinary clinical P. aeruginosa isolates (n=24) to polymyxin antibiotics, colistin (polymyxin E) and polymyxin B, by broth micro dilution and showed that the MICs for polymyxin B to be significantly higher than in a panel of human P. aeruginosa isolates (n= 37). Resistance to other antibiotics used in human medicine was low but higher levels of resistance were detected to ticarcillin (21%), and also to marbofloxacin (21%) and enrofloxacin (33%), these being two widely used veterinary antibiotics. Using the array tube typing method, the P. aeruginosa veterinary isolates were found to be distributed throughout the P. aeruginosa population, with shared array types from human infections such as keratitis and respiratory infections. Using whole genome sequencing on a limited subset of isolates, the veterinary isolates were generally clustered within the main P. aeruginosa population; however one isolate, did not 6 cluster with any other previously sequenced isolate. The genome sequencing also revealed that isolates had mutations in genes associated with polymyxin resistance and other antimicrobial resistance-related genes. These findings may suggest that treating animal infections with antimicrobials could lead to resistance in isolates capable of causing human infections. The prevalence of resistance to beta-lactams, aminoglycosides and fluoroquinolones in isolates from companion animals particularly in P. aeruginosa is a relatively understudied area. Here, the resistance characteristics of a set of P. aeruginosa isolates from companion animals (n=106), collected, at the Veterinary Diagnostic laboratory (VDL) at the Small Animal Teaching Hospital, Leahurst (University of Liverpool, UK) was investigated. Several resistance genes including those relating to ESBLs (blaTEM, blaSHV and blaOXA) and those relating to fluroquinolone resistance (qnr) were identified. In particular the identification of qnrA and qnrB genes in P.aeruginosa isolates of companion animal origin is a novel finding with no known reports to current date in the UK. Of the 8 confirmed sequenced positive amplicons they comprised 7 different isolates all canine in origin. Multidrug resistance was also demonstrated among some isolates. These findings
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