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Isolation and Characterisation of Imipenem-Resistant Bacteria from Natural Environments and Clinical Settings

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Isolation and Characterisation of Imipenem-Resistant Bacteria from Natural Environments and Clinical Settings THE UNIVERSITY OF HULL Isolation and characterisation of imipenem-resistant bacteria from natural environments and clinical settings being a Thesis submitted for the Degree of Doctor of Philosophy in Biological Sciences (Molecular Microbiology) in the University of Hull by Fahd Alkhaleefah BSc. MSc. March 2015 Dedication I would like to dedicate this work to my father, who sadly passed away during my postgraduate studies, and also to my mother, for all the unconditional love and support they have given me throughout my life. To my wife, Abeer, for her constant love and companionship, and for sharing the good times as well as the bad during our time away from home. To Yara and Asil, my children, for bringing so much joy and happiness into my life. To my brothers and sisters, for always being there for me and cheerfully giving freely of their love and encouragement. To all my friends in Hull, for their warmth and kindness during the years I have been here, and for all the great times we have had together. ii Abstract The development and spread of bacterial resistance to antimicrobials is now recognised as a key threat to public health and society. A small number of antimicrobials, including imipenem and vancomycin, are now considered to be the drugs of ‘last resort’ for treating antibiotic resistant bacteria. This study investigates and characterises antibiotic (imipenem) resistant bacteria in environmental and clinical samples from the U.K. Imipenem resistant (ImR) bacteria were isolated and characterised from river water samples from East Yorkshire and soil samples from Lincolnshire. ImR clinical isolates from different hospitals (York, Sheffield and Hull) were also characterised. Phenotypic resistance to imipenem was observed in 11.2% (75/670 CFU ml-1), 13.3% (145.35 x 105/ 109.1 x 106 CFU g-1) and 38.5% (42/109) of water, soil and clinical bacterial isolates, respectively.The minimum inhibitory concentrations (MICs) of the clinical isolates were generally higher (> 32 mg L-1 in 71.4% of isolates) than those of the environmental isolates, which were around 4 mg L-1 in 63.4% of water isolates and in 42.7% of soil isolates. β-lactamase activity studies showed that the most common β-lactamases among the environmental isolates were class B metallo β-lactamases (MBLs) (84.2%), while class A Klebsiella pneumoniae carbapenemases (KPCs) (40.5%) were the most common β-lactamases observed in the clinical isolates. Higher frequencies of multi- drug resistant (MDR) patterns were detected among the environmental isolates than among the clinical strains. Sequencing of 16S rRNA genes identified 30 (17 species), 96 (27 species), and 42 (11 species) ImR bacteria in water, soil and clinical samples, respectively. The most abundant genera identified were Caulobacter (36.7%), Stenotrophomonas (44.8%) and Stenotrophomonas (40.5%) from water, soil and clinical environments, respectively. PCR products were generated from ImR clinical isolates and some of the environmental isolates using primers targeting β- lactamase genes. Sequence analysis of these products from clinical isolates showed that they were specific and related to β-lactamase genes. However, the products from environmental isolates were not related to known genes characterised from antibiotic resistant clinically important bacteria. This suggests that there is a potentially large and divergent gene pool encoding for imipenem ressitance within natural environments, and that river water and agricultural soil are important as reservoirs of novel antibiotic resistance. Genome sequencing was used to characterise 8 MDR Stenotrophomonas spp. isolates from water, soil and clinical samples. This analysis showed the detection of β-lactamases genes (between 8 and 15 genes per isolate) including class A (L2), B (L1) and C (AmpC), fluoroquinolones resistance genes (between 4-8 genes per isolate), and genes encoding MDR efflux pumps (between 23-32 genes per isolate). Antibiotic resistance genes for other antimicrobials were also observed in small numbers; these represented aminoglycoside, sulphonamide and tetracycline resistance. Genes encoding resistance to heavy metal resistance (between 13-27 genes per isolate) were also observed. Overall, this research has demonstrated the widespread presence of imipenem resistant bacteria in environmental and clinical settings, carrying multiple resistances to other antibiotics. In particular, imipenem resistant Stenotrophomonas spp. were present in all of the environments studied and these bacteria were found to harbour multiple and diverse antibiotic resistance genes, that differed between isolates from environmental and clinical origins. iii Acknowledgements I would like to express my sincere gratitude to my supervisor, Professor Mark Osborn, for all he has done to help this study come to fruition. I would like to thank Mark especially for his inspiration and guidance during each stage of the project and for patiently and meticulously reading through my work. He has always been more than generous with his experience and knowledge. Special thanks are also due to Mrs Christine Murphy for her constant support and encouragement throughout this study. Christine has always been there for me whenever I have needed advice and nothing was ever too much trouble for her. I would also like to thank Dr Jennifer Waby for her advice and encouragement and for engaging me in various academic activities. Tremendous thanks also go to Professor John Greenman, who has been a major help in making practical arrangements and ensuring that everything ran smoothly for me. I would also like to thank Dr Gavin Paterson for taking an interest in my work and for reassuring me in some difficult moments. I am greatly indebted to my employer and sponsor, the Ministry of Health in Saudi Arabia, for giving me this wonderful opportunity to study at a UK university and for financially supporting me during the whole process. Thanks also go to the Ministry of Education in Saudi Arabia and the Cultural Bureau of Saudi Arabia in London for all their help in managing the practical matters involved in living and studying abroad. Finally, I would like to thank the University of Hull and the School of Biological, Biomedical and Environmental Sciences for the many ways in which they have helped me and made me feel at home. iv Abbreviations Abbreviation Description AMR Antimicrobial drug resistance AR Antibiotic resistant ARG Antibiotic resistance gene ART Anti-retroviral therapy ATM Aztreonam ATP Adenosine tri-phosphate BA Boronic acid BLAST Basic Local Alignment Search Tool CAZ Ceftazidime CDST Combined disc synergy test CF Cystic fibrosis CFU Colony-forming unit CGE Centre for Genomic Epidemiology CIP Ciprofloxacin CN Gentamicin CPE Carbapenemase-producing enterobacteria CRAB Carbapenem-resistant Acinetobacter baumanii CRKP Carbapenem-resistant Klebsiella pneumoniae DNA Deoxyribonucleic acid DPA Dipicolinic acid EDTA Ethylenediaminetetraacetic acid ESBL Extended-spectrum β-lactamase GC-content Guanine-cytosine content gDNA Genomic DNA GI Genomic island GISA Glycopeptide-intermediate resistant Staphylococcus aureus GNSA Gram-negative selective agar v Abbreviation Description HAI Hospital-acquired infection HGT Horizontal gene transfer Im/IMP/IPM Imipenem ImR Imipenem-resistant IS Insertion sequence KPC Klebsiella pneumoniae carbapenemase LEV Levofloxacin MBL Metallo-β-lactamase MCA MacConkey agar MDR Multi-drug resistant MEM/MER Meropenem MGE Mobile genetic element MH Minocycline MHT Modified Hodge test MIC Minimum inhibitory concentration MLST Multi-Locus Sequence Typing MRG Heavy metal resistance gene MRSA Methicillin-resistant Staphylococcus aureus MSSA Methicillin-sensitive Staphylococcus aureus NDM New Delhi metallo-β-lactamase NGS Next-generation sequencing NPK Nitrogen, phosphorus and potassium OD Optical density ORF Open reading frame OXA Oxacillin PABA Para-aminobenzoic acid PBP Penicillin-binding protein PCA Plate count agar PCR Polymerase chain reaction vi Abbreviation Description PEG Protein encoding gene PIA Pseudomonas isolation agar RAST Rapid Annotation using Subsystem Technology RNA Ribonucleic acid RND Resistance nodulation-cell division SCV Small colony variant SHV Sulfhdryl variable SXT Co-trimoxazole TBDR TonB-dependent receptor TE Tetracycline TIM Ticarcillin-clavulanate TSA Tryptone soya agar TTC Tergitol-7-agar TVC Total viable bacterial count UTI Urinary tract infection VIM Verona integron–encoded metallo-β-lactamase VISA Vancomycin- intermediate resistant Staphylococcus aureus Vm Vancomycin VmR Vancomycin-resistant VRE Vancomycin-resistant Enterococci VRSA Vancomycin-resistant Staphylococcus aureus W Trimethoprim XDR Extensively drug-resistant vii Table of Contents Dedication _______________________________________________________ ii Abstract ________________________________________________________ iii Acknowledgements _______________________________________________ iv Abbreviations ____________________________________________________ v Table of Contents _______________________________________________ viii List of Tables ____________________________________________________ xii List of Figures __________________________________________________ xiv CHAPTER 1: INTRODUCTION ________________________________ 1 1.1 Overview _____________________________________________________ 1 1.2 Antimicrobial agents ___________________________________________ 4 1.3 Classification and mechanism of action of antimicrobials _____________ 5 1.3.1 Inhibitors of bacterial cell wall synthesis ..........................................................................
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