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Molecular Epidemiology of Staphylococcus Epidermidis in Prosthetic Joint Infections

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Molecular Epidemiology of Staphylococcus Epidermidis in Prosthetic Joint Infections Molecular epidemiology of Staphylococcus epidermidis in prosthetic joint infections To my family Örebro Studies in Medicine 203 EMELI MÅNSSON Molecular epidemiology of Staphylococcus epidermidis in prosthetic joint infections © Emeli Månsson, 2019 Title: Molecular epidemiology of Staphylococcus epidermidis in prosthetic joint infections Publisher: Örebro University 2019 www.oru.se/publikationer Print: Örebro University, Repro 10/2019 ISSN 1652-4063 ISBN 978-91-7529-309-7 Abstract Emeli Månsson (2019): Molecular epidemiology of Staphylococcus epidermidis in prosthetic joint infections. Örebro Studies in Medicine 203. Staphylococcus epidermidis is ubiquitous in the human microbiota, but also an important pathogen in healthcare-associated infections, such as prosthetic joint infections (PJIs). In this thesis, aspects of the molecular epidemiology of S. epidermidis in PJIs were investigated with the aim of improving our understanding of the pre- and perioperative measures required to reduce the incidence of S. epidermidis PJIs. In Paper I, S. epidermidis retrieved from air sampling in the operating field during arthroplasty was characterized by multilocus sequence typ- ing and antibiotic susceptibility testing. No isolates belonging to se- quence types (STs) 2 and 215, previously associated with PJIs, were found in the air of the operating field. During air sampling, several Staphylococcus pettenkoferi isolates were identified, and as a spin-off of Paper I, the genomic relatedness of these isolates to S. pettenkoferi iso- lates from blood cultures was described in Paper II. In Paper III, genetic traits distinguishing S. epidermidis isolated from PJIs were determined using genome-wide association study accounting for population effects after whole-genome sequencing (WGS) of a popu- lation-based 10-year collection of S. epidermidis isolates from PJIs and of nasal isolates retrieved from patients scheduled for arthroplasty. Genes associated with antimicrobial agents used for prophylaxis in ar- throplasty, i.e., beta-lactam antibiotics, aminoglycosides, and chlorhexi- dine, were associated with PJI origin. S. epidermidis from PJIs were dominated by the ST2a, ST2b, ST5, and ST215 lineages. In Paper IV, selective agar plates were used to investigate colonization with methicillin resistant S. epidermidis (MRSE) in patients scheduled for arthroplasty. MRSE were further characterized by WGS. A subset of patients was found to harbour PJI-associated S. epidermidis lineages in their microbiota before hospitalization, but no isolates belonging to the ST2a lineage nor any rifampicin-resistant isolates were retrieved. Keywords: Staphylococcus epidermidis, molecular epidemiology, prosthetic joint infections, whole genome sequencing, Staphylococcus pettenkoferi Emeli Månsson, School of Medical Sciences, Örebro University, SE-70182 Örebro, Sweden, [email protected] Table of Contents LIST OF ORIGINAL PAPERS .................................................................. 9 LIST OF ABBREVIATIONS ................................................................... 11 INTRODUCTION .................................................................................. 13 Coagulase negative staphylococci ............................................................ 15 Staphylococcus pettenkoferi ................................................................ 16 Introduction to genomic analyses in molecular epidemidology studies 17 Whole genome sequencing (WGS) .................................................... 18 Analysis of WGS data – bioinformatics ............................................. 20 Staphylococcal Casette Chromosome mec (SCCmec) .......................... 22 Staphylococcus epidermidis – a friend and a foe ..................................... 22 S. epidermidis in the human microbiota .............................................. 23 S. epidermidis in clinical infections...................................................... 24 Molecular epidemiology of S. epidermidis ........................................ 25 Molecular typing of S. epidermidis from PJIs .................................. 25 Biofilm formation by S. epidermidis .................................................... 26 Quorum sensing - molecular crosstalk within the biofilm ................. 27 Attenuated host immune response in biofilms ................................... 28 Recalcitrance towards antimicrobial treatment ................................. 28 Antibiotic susceptibility testing (AST) of S. epidermidis ...................... 28 WGS in AST...................................................................................... 29 What discriminates clinical S. epidermidis from commensal S. epidermidis isolates? ....................................................................... 30 Biofilm formation ............................................................................. 30 Antimicrobial resistance, IS256 and sesI ........................................... 30 fdh and ACME - markers of commensalism? .................................... 31 Hip- and knee prosthetic joint infections with S. epidermidis .................. 32 Diagnostic criteria for S. epidermidis PJI ............................................. 32 Classification of PJIs ........................................................................... 35 Incidence of hip and knee S. epidermidis PJIs ...................................... 35 Pathogenesis of S. epidermidis PJIs...................................................... 36 Treatment of S. epidermidis PJIs ......................................................... 38 Morbidity and mortality in PJIs .......................................................... 41 Preventive strategies in prosthetic joint surgery in Sweden .................. 42 Summary of introduction ........................................................................ 43 AIMS ....................................................................................................... 44 MATERIALS AND METHODS ............................................................. 45 Sampling of patients (Paper III-IV) .......................................................... 45 Intraoperative air sampling (Paper I) ....................................................... 47 Bacterial isolates (Paper I-IV) .................................................................. 47 Paper I ............................................................................................. 47 Paper II ............................................................................................ 47 Paper III .......................................................................................... 48 Paper IV .......................................................................................... 48 Species identification (Paper I-IV) ............................................................ 49 MALDI-TOF MS (Paper I-IV) ............................................................. 49 rpoB gene sequencing (Paper II) .......................................................... 49 16S rRNA gene sequencing (Paper I) ................................................... 50 Antimicrobial susceptibility testing (Paper I-III) ...................................... 50 Genotyping methods ............................................................................... 50 MLST (Paper I,III-IV) .......................................................................... 50 Rep-PCR typing (Paper II) ................................................................... 51 WGS and analysis of WGS data (Paper II-IV) .......................................... 51 DNA extraction and library preparation ............................................. 51 Genome sequencing and quality control .............................................. 52 Publically available genome sequences used in this thesis (Paper II-IV) 52 Phylogenetic relationships ................................................................... 52 Genome-wide analysis study (GWAS) (Paper III) ................................ 53 Genotypic antimicrobial resistance (Paper II-IV) ................................. 54 SCCmec diversity (Paper III) ............................................................. 54 Genes associated with biofilm, virulence and commensalism (Paper III, IV, additional data) ............................................................. 54 Digital DNA:DNA hybridization (additional data) ............................. 55 Phenotypic biofilm production (study II) ................................................. 55 Ethical considerations .............................................................................. 56 Statistics .................................................................................................. 57 RESULTS AND DISCUSSION ................................................................ 58 Molecular epidemiology of S. epidermidis in relation to PJIs (I, III, IV) .. 58 Clonal relatedness of S. epidermidis isolated from PJIs ....................... 58 Swedish PJI isolates ........................................................................... 58 International data .............................................................................. 61 Genetic diversity of S. epidermidis retrieved from the microbiota of patients scheduled for prosthetic joint surgery (Paper III, IV) .............. 65 Nasal S. epidermidis retrieved from standard culture medium .......... 65 Nasal and skin S. epidermidis retrieved from media
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