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Epidemiology and Pathogenesis of Moraxella Catarrhalis Colonization and Infection

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Epidemiology and Pathogenesis of Moraxella Catarrhalis Colonization and Infection Epidemiology and Pathogenesis of Moraxella catarrhalis Colonization and Infection Suzanne J.C. Verhaegh ISBN: 978-94-6169-043-2 © S.J.C. Verhaegh, 2011 All rights reserved. No part of this thesis may be reproduced or transmitted in any form or by means without prior permission of the author, or where appropriate, the publisher of the articles. Printing of this thesis was financially supported by (in alphabetical order): BD Diagnostics-Diagnostic Systems, bioMérieux Benelux BV, GlaxoSmithKline, The Netherlands Society of Medical Microbiology (NVMM) and The Netherlands Society for Microbiology (NVvM), Merck Sharp & Dohme BV, Oxoid BV Layout and printing: Optima Grafische Communicatie, Rotterdam, The Netherlands Cover design: Eline S. Klaassens Epidemiology and Pathogenesis of Moraxella catarrhalis Colonization and Infection Epidemiologie en pathogenese van Moraxella catarrhalis kolonisatie en infectie Proefschrift ter verkrijging van de graad van doctor aan de Erasmus Universiteit Rotterdam op gezag van de rector magnificus Prof.dr. H.G. Schmidt en volgens besluit van het College voor Promoties. De openbare verdediging zal plaatsvinden op woensdag 1 juni 2011 om 13.30 uur door Suzanne Johanna Christina Verhaegh geboren te Tegelen Promotiecommissie Promotor: Prof.dr.dr. A. van Belkum Overige leden: Prof.dr. H.A. Verbrugh Prof.dr. H.A. Moll Prof.dr. P.W.M. Hermans Copromotor: Dr. J.P. Hays Contents Introduction Chapter 1 General introduction, aim and outline of the thesis 9 Chapter 2 Moraxella catarrhalis: a human pathogen 13 Dynamics of Moraxella catarrhalis colonization and infection Chapter 3 Determinants of Moraxella catarrhalis colonization in healthy 33 Dutch children during the first 14 months of life Chapter 4 Colonization of healthy children by Moraxella catarrhalis is 47 characterized by genotype heterogeneity, virulence gene diversity, and co-colonization with Haemophilus influenzae Chapter 5 Age-related genotypic and phenotypic differences in Moraxella 69 catarrhalis isolates from children and adults presenting with respiratory disease in 2001-2002 Chapter 6 Microbial analysis does not facilitate the differentiation of child- 85 hood recurrent acute otitis media (rAOM) from chronic otitis media with effusion (COME) Chapter 7 Differential virulence gene expression of group A Streptococcus 103 serotype M3 in response to co-culture with Moraxella catarrhalis Humoral immune response Chapter 8 Temporal development of the humoral immune response to 121 surface antigens of Moraxella catarrhalis in young infants Chapter 9 Comparative analysis of the humoral immune response to 139 Moraxella catarrhalis and Streptococcus pneumoniae surface antigens in children suffering from recurrent acute otitis media (rAOM) and chronic otitis media with effusion (COME) Contents 5 General discussion Chapter 10 Summarizing discussion 157 Chapter 11 Nederlandse samenvatting 171 Appendices Dankwoord 181 Curriculum Vitae 187 List of publications 189 PhD portfolio 191 6 Contents Introduction Chapter 1 General introduction, aim and outline of the thesis General introduction Moraxella catarrhalis is part of the normal bacterial flora in the nasopharynx of children, although over the past two decades, it has emerged as a significant bacterial pathogen and not simply a commensal colonizer. The bacterium rapidly colonizes the nasopharynx soon after birth and many factors affect nasopharyngeal carriage of this human-specific pathogen, including for example, the presence of siblings, day-care attendance and re- spiratory illness. Otitis media (OM) is a particularly important respiratory illness during early childhood and the primary reason for children to visit a physician. The most com- mon bacterial species cultured from the nasopharynx of children during OM episodes are Streptococcus pneumoniae, Haemophilus influenzae and M. catarrhalis, either as single pathogens or as co-cultures, with the patterns of nasopharyngeal colonization by microorganisms being important determinants for OM disease. There is increasing information regarding the biological mechanisms facilitating M. catarrhalis-mediated colonization and disease development, with most publications stressing the importance of bacterial adherence as an essential step in this process. Treatment of OM is not always appropriate, and the long-term overuse of antibiotics in OM reduces the effectiveness of treatment and places children at an increased risk of antibiotic-resistant infections. Because there is currently no ideal treatment for OM, an alternative to the use of antibiotics is vaccination. To date, several M. catarrhalis vaccine candidates have been described, which may be effective in reducing the burden of OM disease. The challenge in identifying potential vaccine candidates for M. catarrhalis lies in identifying antigens that are able to generate an appropriate immune response to prevent colonization and infection. However, there is no licensed vaccine available against M. catarrhalis, and none of the putative vaccine candidates so far described have progressed to clinical trials. Aim and outline of the thesis The aim of this thesis is to help understand the epidemiology and pathogenesis of M. catarrhalis colonization and infection, with special emphasis on isolate variation, the humoral immune response and novel immunologically relevant vaccine candidates of M. catarrhalis. Chapter 1 11 In this respect, Chapter 2 provides a detailed description of our current knowledge regarding M. catarrhalis as a human pathogen and the treatment and management of this organism. The subsequent seven chapters are then divided into two main themes, relating to the dynamics of M. catarrhalis colonization and infection (Chapters 3 – 7) and the humoral immune response (Chapter 8 – 9). In Chapter 3, determinants of M. catarrhalis colonization in healthy Dutch children during the first months of life were defined, whereas in Chapter 4, pulsed-field gel electrophoresis, PCR and PCR-RFLP are used to determine the genotypic relationship be- tween colonizing M. catarrhalis strains of healthy children, and to study virulence gene diversity. Further, co-colonization with H. influenzae was also investigated. In Chapter 5, the age-related genotypic and phenotypic differences in M. catarrhalis isolates from children and adults presenting with respiratory disease were investigated. Chapter 6 gives an overview of a prospective study that looked into the differences in the presence of bacteria and viruses in the middle ear and nasopharynx of children diagnosed with recurrent acute otitis media (rAOM) and chronic otitis media with effusion (COME). The role of the major bacterial pathogens S. pneumoniae, H. influenzae and M. catarrhalis, in the absence or presence of 15 respiratory viruses, was studied in detail. In fact, previous research has shown that bacterial co-colonization does lead to increased colo- nization and infection, with S. pneumoniae, H. influenzae and M. catarrhalis being the predominant co-colonizing bacterial organisms associated with OM. However, group A Streptococcus (GAS) may also be included as one of the most frequent causative agents of OM, especially with reference to the increasing importance of GAS in OM disease in Eastern Europe. Therefore, in Chapter 7, studies were performed to investigate the effect of M. catarrhalis co-culture on GAS gene expression, particularly with respect to the expression of GAS virulence genes. Relatively little is known about the development of the humoral immune response to M. catarrhalis surface antigen vaccine candidates within the first few years of life in healthy and sick children. In this respect, the studies presented in Chapter 8 and 9 were established in order to study the humoral immune response generated against the currently identified surface antigens of M. catarrhalis (Chapter 8 and 9) and S. pneumoniae (Chapter 9). The relationship between colonization and immune response was also investigated. Finally, Chapter 10 gives a summary of the research presented within this thesis and discusses the findings with respect toM. catarrhalis vaccine development. 12 Chapter 1 Chapter 2 Moraxella catarrhalis: a human pathogen Adapted from: Suzanne J.C. Verhaegh and John P. Hays. Chapter 80 Moraxella. In: Liu, D. (ed), Mo- lecular Detection of Human Bacterial Pathogens. 2011. Taylor & Francis CRC Press, Boca Raton, FL, USA. In press. The genus Moraxella The genus Moraxella belongs to the family Moraxellaceae, which includes the closely related genera Acinetobacter and Psychrobacter. The Moraxella genus itself currently contains 15 different species, including M. lacunata, M. atlantae, M. boevrei, M. bovis, M. canis, M. caprae, M. catarrhalis, M. caviae, M. cuniculi, M. equi, M. lincolnii, M. nonliquefaciens, M. osloensis, M. ovis and M. saccharolytica [1]. Recently, M. plurani- malium has been described as a new species of the genus Moraxella after its isolation from sheep and pigs [2]. Although all of these 16 species have been classified within the genus Moraxella, the classification of the Moraxellaceae family is still not definitive but continuously evolving. For example, molecular systematic studies (of which 16S ribosomal RNA (rRNA) gene sequencing has long been the ‘gold standard’) has led to the re-classification of Riemerella anatipestifer, Psychrobacter phenylpyruvicus and Oligella urethralis, which were formally known as Moraxella anatipestifer, Moraxella phenylpyruvica and Moraxella urethralis, respectively [1, 3]. Of the 16 Moraxella species,
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