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Genomic Surveillance of Methicillin-Resistant Staphylococcus Aureus at Local, Regional and National Levels Michelle Suzanne Tole

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Genomic Surveillance of Methicillin-Resistant Staphylococcus Aureus at Local, Regional and National Levels Michelle Suzanne Tole Genomic surveillance of methicillin-resistant Staphylococcus aureus at local, regional and national levels Michelle Suzanne Toleman Darwin College Department of Medicine Wellcome Sanger Institute University of Cambridge June 2019 This dissertation is submitted for the degree of Doctor of Philosophy Declaration This thesis describes work carried out between January 2015 and June 2019 under the supervision of Professor Sharon Peacock at the Department of Medicine, University of Cambridge and Professor Julian Parkhill at the Wellcome Sanger Institute. This dissertation is the result of my own work. Any work that is the outcome of collaboration is indicated in the collaborative contributions section of the text. This work is not substantially the same as any that I have submitted, or, is being concurrently submitted for a degree or diploma or other qualification at the University of Cambridge or any other University or similar institution except as specified in the text. No substantial part of my dissertation has already been submitted, or, is being concurrently submitted for any such degree, diploma or other qualification at the University of Cambridge or any other University or similar institution except as specified in the text. This work contains less than 60,000 words. Michelle Suzanne Toleman, June 2019 ii Genomic surveillance of methicillin-resistant Staphylococcus aureus at local, regional and national levels Michelle S. Toleman Abstract Methicillin-resistant Staphylococcus aureus (MRSA) is a major cause of hospital-acquired infection, which is associated with increased cost and length of hospital stays and substantial morbidity and mortality. The rapid progression of whole-genome sequencing (WGS) technologies over the past decade has provided highly detailed and discriminatory insights into the epidemiology of MRSA. However, WGS is still not implemented in the routine surveillance of MRSA at a local, regional or national level. This thesis applies WGS to a number of questions and populations to describe its benefits. Standard infection control investigation commonly uses the antimicrobial susceptibility patterns (ASPs, patterns of susceptibility and resistance to commonly used antibiotics) of MRSA as a surrogate for bacterial relatedness. As they are readily available, ASPs are often combined with patient movement to evaluate putative MRSA outbreaks in hospitals. The accuracy of this method was evaluated by comparing linked cases based on MRSA ASPs versus linked cases based on whole-genome relatedness, using data from a year-long prospective observational cohort study of 1,465 MRSA-positive individuals. The sensitivity and specificity of ASP in the presence of a direct ward contact was 44% and 85%, respectively; in the presence of a shared residential post code, the sensitivity and specificity of ASP is 59% and 76%, respectively. This demonstrates that compared to WGS plus epidemiology, ASP and epidemiology does not reliably identify or refute transmission events. A lineage referred to as epidemic (E)-MRSA15 is largely considered to be associated with hospital settings, but an epidemiological and genomic investigation of a MRSA outbreak in a General Practice (GP) identified 15 people who were E-MRSA15 positive, the majority of which shared a link to a leg ulcer/podiatry clinic in the GP surgery. The outbreak had not been detected previously, and was only identified post-hoc from MRSA sequence data, highlighting the importance of MRSA sequencing to detect otherwise cryptic community outbreaks. iii The utility of WGS for the investigation of regional MRSA epidemiology was explored for two potentially high-risk MRSA lineages (USA300 and ST2371) that are otherwise unmonitored by current surveillance. Screening the genomes of MRSA isolated from 1,465 people identified over a 12-month period demonstrated that 4.2% of cases were positive for MRSA USA300, with multiple introductions and household transmissions identified. Five people were positive for ST2371, all of whom had a direct or indirect link to a substantial outbreak in an intensive care unit at Addenbrooke’s Hospital in 2011, thus confirming the value of WGS in regional epidemiological investigations. The feasibility and utility of incorporating WGS into routine national MRSA surveillance was evaluated through a combined epidemiological and genomic survey of MRSA bacteraemia undertaken in England over a one-year period. This captured 903 reported cases of MRSA bacteraemia, with 425 isolates available for sequencing. Almost two thirds of isolates were assigned to multi-locus sequence type clonal complex (CC) 22. The addition of MRSA genomes from published outbreak investigations showed that the study genomes could provide context for outbreak isolates and supported cluster identification. Potentially high-risk lineages were also detected. These findings support the integration of epidemiological and genomic surveillance for MRSA bacteraemia as a first step towards a comprehensive national surveillance programme. iv Acknowledgements I would like to thank Professors Sharon Peacock and Julian Parkhill for granting me the opportunity to undertake this work under their inspirational supervision. Thank you both for your valuable time, support, guidance and kindness throughout. Estée Török has been an excellent mentor and provided generous support throughout my PhD. Similarly, Sandra Reuter and Emmeline Watkins have provided ongoing friendship, advice and inspiration. Members of the Peacock and Török research groups have kindly supported this work, in particular Ewan Harrison, Francesc Coll, Hayley Wilson, Beth Blane, and Carol Churcher. I am grateful to Nicholas Brown and David Aanensen for their input. The Pathogen Genomics team at the Wellcome Sanger Institute has provided essential bioinformatics expertise, in particular, Simon Harris (developer of most of the bioinformatic pipelines used in this work), Sophia David, Dorota Jamrozy, Izzy Everall, Rebecca Gladstone, Kim Judge and Theresa Feltwell. I also acknowledge the work of the Sanger Institute’s core Pathogen Production Groups and Pathogen Informatics Group. I am also grateful to the Wellcome Trust PhD Programme for Clinicians programme at the University of Cambridge for providing me with funding for this work. I would like to thank the microbiology consultants who have supervised my training, in particular Martin Williams and Marina Morgan for their support during my PhD studies. Finally, I would like to thank my family and friends for their inspiration and encouragement. v Collaborative contributions The collaborative contributions to this work are listed by chapter. Chapter 3. Francesc Coll provided data from the Cambridgeshire prospective MRSA study. I undertook the analysis and interpretation of data. Sandra Reuter, Julian Parkhill and Emmeline Watkins provided valuable guidance. Sharon Peacock and Ewan Harrison supervised the study. Chapter 4. USA300 study: Beth Blane conducted the laboratory work. Nicholas Brown provided clinical laboratory support. I undertook the phylogenetic and epidemiological analysis of data. Ewan Harrison and Sandra Reuter provided valuable guidance. Francesc Coll generated Figure 4.1. Sharon Peacock, Estée Török and Julian Parkhill supervised the study. ST2371 study: Beth Blane conducted the laboratory work. Francesc Coll undertook the phylogenetic analysis as a training aid, and generated Figure 4.5 and 4.6. I collected and analysed patient level epidemiological and clinical data. Ewan Harrison and Sandra Reuter provided valuable advice. Sharon Peacock supervised the study. Chapter 5. Outbreak meetings were chaired by Nicholas Brown and were regularly attended by myself alongside Emmeline Watkins, Belinda Sadler, Bernadette Nazareth, Rachel Thaxter and the practice manager. Beth Blane cultured isolates and extracted DNA. I carried out sampling of staff and the environment on-site with Belinda Sadler. Environmental samples were processed in the clinical microbiology laboratory at CUH. Bernadette Nazareth collated the patient information sheet and consent form. Patient data was extracted by the practice manager. Epidemiological analysis was undertaken by myself and Emmeline Watkins. I conducted the bioinformatic analysis, interpreted the data and generated the figures. Francesc Coll, Ewan Harrison, Jill Eastment, Lynn Rodrigues, Estée Török, Sandra vi Reuter and Dorota Jamrozy provided valuable advice. Sharon Peacock and Julian Parkhill supervised this work. Chapter 6. Beth Blane and Hayley Wilson performed the laboratory work in Cambridge. Russell Hope and Angela Kearns co-ordinated the collection and characterisation of isolates and provided the epidemiological and laboratory data from PHE Colindale. Francesc Coll provided data from the Cambridgeshire MRSA prospective study. I performed epidemiological and bioinformatic analyses and produced the figures. Assistance was provided by Sandra Reuter, and from Dorota Jamrozy regarding in silico spa-typing. Ewan Harrison, Sharon Peacock and Julian Parkhill provided valuable advice. Estée Török supervised this work. vii Table of Contents CHAPTER 1. INTRODUCTION 1 1.1. STAPHYLOCOCCUS AUREUS: MICROBIOLOGY 1 1.1.1. Microbiological Characteristics and Identification 1 1.1.2. Colonisation and Disease 1 1.1.3. Methicillin Resistance 2 1.2. METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS 4 1.2.1. Clinical Features of MRSA Infection 4 1.2.3. History of MRSA in England 4 1.2.4. Current Epidemiology of MRSA Bacteraemia in England 6 1.3. IDENTIFICATION
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