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Staphylococcus Aureus in Companion Animals: an Infection Source for the Community?

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Staphylococcus Aureus in Companion Animals: an Infection Source for the Community? Aus dem Institut für Mikrobiologie und Tierseuchen des Fachbereichs Veterinärmedizin der Freien Universität Berlin Staphylococcus aureus in companion animals: An infection source for the community? Inaugural-Dissertation zur Erlangung des Grades eines PhD of Biomedical Sciences an der Freien Universität Berlin vorgelegt von Szilvia Vincze Tierärztin aus Budapest Berlin 2014 Journal-Nr. 3756 Gedruckt mit Genehmigung des Fachbereichs Veterinärmedizin der Freien Universität Berlin Dekan: Univ.-Prof. Dr. Jürgen Zentek Erster Gutachter: Univ.-Prof. Dr. Lothar H. Wieler Zweiter Gutachter: Univ.-Prof. Dr. Barbara Kohn Dritter Gutachter: Univ.-Prof. Dr. Uwe Rösler Deskriptoren (nach CAB-Thesaurus): Staphylococcus aureus, methicillin-resistant Staphylococcus aureus, cats, dogs, horses, epidemiology, wound infections, zoonoses, genotypic variation, genotypes Tag der Promotion: 27.02.2015 Bibliografische Information der Deutschen Nationalbibliothek Die Deutsche Nationalbibliothek verzeichnet diese Publikation in der Deutschen Nationalbibliografie; detaillierte bibliografische Daten sind im Internet über <http://dnb.ddb.de> abrufbar. ISBN: 978-3-86387-578-7 Zugl.: Berlin, Freie Univ., Diss., 2014 Dissertation, Freie Universität Berlin D 188 Dieses Werk ist urheberrechtlich geschützt. Alle Rechte, auch die der Übersetzung, des Nachdruckes und der Vervielfältigung des Buches, oder Teilen daraus, vorbehalten. Kein Teil des Werkes darf ohne schriftliche Genehmigung des Verlages in irgendeiner Form reproduziert oder unter Verwendung elektronischer Systeme verarbeitet, vervielfältigt oder verbreitet werden. Die Wiedergabe von Gebrauchsnamen, Warenbezeichnungen, usw. in diesem Werk berechtigt auch ohne besondere Kennzeichnung nicht zu der Annahme, dass solche Namen im Sinne der Warenzeichen- und Markenschutz-Gesetzgebung als frei zu betrachten wären und daher von jedermann benutzt werden dürfen. This document is protected by copyright law. No part of this document may be reproduced in any form by any means without prior written authorization of the publisher. Alle Rechte vorbehalten | all rights reserved © Mensch und Buch Verlag 2015 Choriner Str. 85 - 10119 Berlin [email protected] – www.menschundbuch.de Content FIGURES 6 TABLES 7 LIST OF ABBREVIATIONS 8 1. INTRODUCTION 10 2. STAPHYLOCOCCUS AUREUS 11 2.1 Taxonomy and characteristics 11 2.2 Relevance of S. aureus in infectious diseases 11 2.3 Resistance mechanisms towards beta-lactam antibiotics 13 2.4 Virulence-associated factors 14 2.5 Epidemiology 16 2.6 Aspects of host specificity in S. aureus 18 2.7 Molecular typing tools 21 2.7.1 Multilocus sequence typing (MLST) 22 2.7.2 Spa typing 24 2.7.3 Pulsed field gel electrophoresis 24 2.7.4 DNA microarray hybridization 25 2.7.5 Whole genome sequencing 25 2.7.6 Comparison of molecular typing tools for genotypic characterization of S. aureus 26 3. PUBLICATIONS 28 3.1 Publication 1 28 3.2 Publication 2 38 3 Content 4. SUPPLEMENT OF UNPUBLISHED DATA 45 4.1 Additional information concerning MRSA isolated from wound infections of dogs, cats and horses 45 4.1.1 PFGE analysis 46 4.1.2 Putative nosocomial relationship of MRSA strains 50 4.1.3 DNA microarray analysis 53 4.2 Investigation of methicillin-susceptible S. aureus isolated from infections of dogs, cats and horses 55 5. DISCUSSION 59 5.1 Host specific aspects of Staphylococcus aureus 59 5.2 S. aureus: lineage specificity 64 5.3 Molecular epidemiology of methicillin-susceptible S. aureus (MSSA) 67 5.4 Relevance of S. aureus as pathogen in companion animals 69 5.5 The role of S. aureus as a nosocomial pathogen in companion animal medicine 71 6. CONCLUSION 73 7. SUMMARY 74 8. ZUSAMMENFASSUNG 76 9. LITERATURE 78 10. APPENDIX I 10.1 Supplementary table S1: PFGE-pattern of MRSA using the macrorestriction enzyme SmaI I 10.2 Supplementary table S2: PFGE-pattern of CC398-MRSA after digestion with ApaI V 10.3 Supplementary table S3: Methicillin-susceptible S. aureus (MSSA) isolated from cats and horses within this study VII 4 Content 11. LIST OF PUBLICATIONS X 12. DANKSAGUNG XIV 13. SELBSTSTÄNDIGKEITSERKLÄRUNG XV 5 Figures Figures Figure 1: Localization of the housekeeping genes used for MLST of S. aureus...................23 Figure 2: Structure of the X region from the spa gene .........................................................24 Figure 3: Macrorestriction analysis of all CC22-MRSA, spa type t032. ................................48 Figure 4: Macrorestriction analysis of all CC5-MRSA, spa type t003. ..................................49 Figure 5: Overview: Submission rates of MRSA-positive wound samples per veterinary institution. ............................................................................................................50 Figure 6: PFGE analysis of 11 isolates from veterinary setting A (Schleswig Holstein) .......... using the macrorestriction enzyme ApaI..............................................................................51 Figure 7: PFGE analysis of 13 MRSA isolates from clinic / practice “B” (Hesse) using the macrorestriction enzyme SmaI. ............................................................................................52 Figure 8: Unrooted tree based on DNA microarray results for 83 MRSA from dog, cat and horse origin. ......................................................................................................................... Figure 9: Lineage-diversity of 50 canine MSSA ..................................................................57 Figure 10: Lineage-diversity of 50 feline MSSA ..................................................................57 Figure 11: Lineage-diversity of 50 equine MSSA ................................................................58 6 Tables Tables Table 1: Overview of important virulence-associated factors................................................16 Table 2: Overview: 241 isolated MRSA grouped according to their clonal complexes. .........46 Table 3: Overview: MSSA strains from dog, cat and horse origin grouped according to their clonal complexes..................................................................................................................56 7 List of Abbreviations List of Abbreviations agr accessory gene regulator arcC housekeeping gene: carbamate kinase aroE housekeeping gene: shikimate dehydrogenase BB Brandenburg bp base pairs BV Bavaria BW Baden-Wuerttemberg CA-MRSA community-associated MRSA CC clonal complex CDC Centers for Disease Control and Prevention chp chemotaxis inhibitory protein DNA deoxyribonucleic acid EHSG extended host spectrum genotype ET exfoliative toxin glpF housekeeping gene: glycerol kinase gmk housekeeping gene: guanylate kinase H Hesse HA-MRSA healthcare-associated MRSA hl hemolysins IEC immune evasion cluster Ig immunglobulin IMT Institute of Microbiology and Epizootics LA-MRSA livestock-associated MRSA LS Lower Saxony Luk leukotoxin MGE mobile genetic elements MLEE multilocus enzyme electrophoresis MLST mulilocus sequence typing MRSA methicillin-resistant S. aureus MSCRAMM microbial surface components recognizing adhesive matrix molecule MSSA methicillin-susceptible S. aureus NGS next generation sequencing NRW North Rhine-Westphalia 8 List of abbreviations orfX open reading frame X PBP penicillin-binding protein PCR polymerase chain reaction PFGE pulsed field gel electrophoresis pta housekeeping gene: phosphate acyltransferase PVL Panton-Valentine leukocidin RKI Robert Koch-Institute RP Rhineland-Palatinate SAg superantigen SaPI S. aureus pathogenicity island SaPIov ovine S. aureus pathogenicity island sak staphylokinase S. aureus Staphylococcus aureus SAXA Saxony Anhalt SCCmec staphylococcal cassette chromosome mec scn staphylococcal complement inhibitor SE staphylococcal enterotoxin SEl staphylococcal enterotoxin-like toxin sea staphylococcal enterotoxin A SH Schleswig Holstein S. hyicus Staphylococcus hyicus SIG Staphylococcus intermedius-group SNP single nucleotide polymorphism spa S. aureus protein A ST sequence type TH Thuringia Tn transposon tpi housekeeping gene: triosephosphate isomerase WGS whole genome sequencing X region highly variable tandem repeat region yqil housekeeping gene: acetyl coenzyme A acyltransferase 9 Introduction 1. Introduction Infections with multi-resistant bacteria are a burden in both human and veterinary medicine. Of special concern are multi-resistant pathogens with a zoonotic potential as they can be transmitted between humans and animals. One prominent example is Staphylococcus (S.) aureus. This opportunistic pathogen is able to cause a broad range of different infections in humans and animals. The occurrence and global spread of methicillin-resistant S. aureus (MRSA) has resulted in a major threat for human healthcare systems due to limited treatment options. While MRSA infections were mainly restricted to humans in the past, multiple case reports raised the awareness of infections with this pathogen in companion animals as a rising therapeutically challenge in veterinary medicine in the late 90s. Since then, several studies investigated the impact of MRSA infection and colonization in animals with regard to the putative zoonotic potential. These surveys focused in particular on the investigation of MRSA isolates from livestock even though S.°aureus-mediated infections were generally also described for various infection sites in companion animals [1]. Nowadays, S. aureus seems to be frequently associated with cases of wound infections in dogs, cats and horses. In contrast to livestock, most companion animals live
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