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Contemporary Syphilis Epidemics: Efforts to Improve Syphilis Diagnostics

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Contemporary Syphilis Epidemics: Efforts to Improve Syphilis Diagnostics Contemporary syphilis epidemics: efforts to improve diagnostics Contemporary syphilis epidemics: efforts to improve syphilis diagnostics Proefschrift voorgelegd tot het behalen van de graad van doctor in de biomedische wetenschappen aan de Universiteit Antwerpen te verdedigen door Kara K. Osbak Kara K.Osbak Promotoren Prof. dr. Chris R. Kenyon Prof. dr. Xaveer van Ostade Faculteit Farmaceutische, Biomedische en Diergeneeskundige Wetenschappen Departement Biomedische Wetenschappen Antwerpen 2017 Faculteit Farmaceutische, Biomedische en Diergeneeskundige Wetenschappen Departement Biomedische Wetenschappen Contemporary syphilis epidemics: efforts to improve syphilis diagnostics ________________________________________ Hedendaagse syfilis epidemieën: inspanningen om de diagnostiek van syfilis te verbeteren Proefschrift voorgelegd tot het behalen van de graad van doctor in de biomedische wetenschappen aan de Universiteit Antwerpen te verdedigen door Kara K. Osbak Promoteren: Prof. dr. Chris R. Kenyon Prof. dr. Xaveer van Ostade Antwerpen, 2017 COLOFON Contemporary syphilis epidemics: efforts to improve syphilis diagnostics. Academic Thesis, University of Antwerp, Antwerp, Belgium. The research described in this thesis was performed at the Institute of Tropical Medicine Antwerp and at the laboratory for Protein Science, Proteomics and Epigenetic Signaling (PPES), University of Antwerp. Kara Osbak was funded by a SOFI-B research grant (Project ID: 757003) from the Flemish Government-Department of Economy, Science & Innovation granted to Chris Kenyon. Front cover photograph: An electron photomicrograph of two spiral shaped Treponema pallidum, magnified 36,000x. (Photo by BSIP/UIG via Getty Images) © K.K. Osbak, Antwerp, 2017. All rights reserved. No parts of this thesis may be reproduced, stored or transmitted in any form or by any means without the prior permission of the author or publishers of the included scientific papers. ⌘ 2 ⌘ Doctoral Committee Promoters: Prof. dr. Chris R. Kenyon Institute of Tropical Medicine Antwerp University of Cape Town Prof. dr. Xaveer van Ostade University of Antwerp Chairman: Prof. dr. Stuart Maudsley University of Antwerp Members: Dr. Alje P. van Dam Public Health Laboratory (GGD) Amsterdam Prof. dr. Dieter Deforce Ghent University Prof. dr. Patrick D'Haese University of Antwerp Prof. dr. Erlangga Yusuf University of Antwerp ⌘ 3 ⌘ ⌘ 4 ⌘ Table of Contents List of abbreviations 7-8 Thesis summary/samenvatting 9-14 Chapter 1. Introduction 15-58 Section I. EPIDEMIOLOGY Chapter 2. The prevalence of syphilis from the early HIV period is 59-70 correlated with peak HIV prevalence at a country level Chapter 3. Superimposing incident STIs on HIV phylogram reveals 71-92 possible misclassification of MSM as heterosexuals in a single-centre cohort in Antwerp, Belgium between 1997-2014 Section II. SYPHILIS DIAGNOSTICS Chapter 4. Characterizing the syphilis-causing Treponema pallidum 93-144 ssp. pallidum proteome using complementary mass spectrometry Chapter 5. Needle lost in the haystack: Multiple Reaction Monitoring 145-176 fails to detect Treponema pallidum candidate protein biomarkers in plasma and urine samples from individuals with syphilis Chapter 6. Evaluation of an automated quantitative latex 177-204 immunoturbidimetric non-treponemal assay for diagnosis and follow-up of syphilis: a prospective cohort study Chapter 7. General Discussion 205-224 Curriculum Vitae 225-228 Acknowledgements 229-231 ⌘ 5 ⌘ ⌘ 6 ⌘ List of Abbreviations ACN Acetonitrile AIDS Acquired immune deficiency syndrome ART Antiretroviral therapy bp Base pair BPG Benzathine penicillin G CDC Centers for Disease Control and Prevention CI Confidence interval CID Collision induced dissociation CSF Cerebrospinal fluid CT Chlamydia trachomatis DDA Data dependent acquisition DIA Data independent acquisition DNA Deoxyribonucleic acid DRT Drug resistance testing DTT Dithiothreitol ECDC European Centre for Disease Prevention and Control EDTA Ethylenediamine tetraacetic acid ELISA Enzyme-linked immunosorbent assay ESI Electrospray ionisation FA Formic acid FDR False discovery rate HIV Human immunodeficiency virus HPLC High performance liquid chromatography hPTPs Isotopically labelled proteotypic surrogate peptides Ig Immunoglobulin IHME Institute for Health Metrics and Evaluation IL Interleukin IQR Interquartile range IT Ion trap ITM Institute of Tropical Medicine Antwerp iTRAQ Isobaric tags for relative and absolute quantification IVDU Intravenous drug user LC Liquid chromatography LC-MS/MS Liquid chromatography–tandem mass spectrometry LOD Limit of detection LTIA Latex turbidimetric immunoassay m/z Mass-to-charge-ratio ⌘ 7 ⌘ MALDI Matrix assisted laser desorption/ionization MRM Multiple reaction monitoring mRNA Messenger RNA MS Mass spectrometry MS/MS Tandem mass spectrometry MTCT Mother to child transmission MudPIT Multidimensional protein identification technology ND Not determined NG Neisseria gonorrhoeae NSAF Normalized spectral abundance factor NTT Nontreponemal test OR Odds ratio ORF Open reading frame PBS Phosphate buffered saline PCR Polymerase chain reaction PMLR Penalized Multinomial Logistic Regression POC Point of care PrEP Pre-exposure prophylaxis PTM Post-translational modification PTP Proteotypic peptide Q Quadrupole RP Reversed phase RPR Rapid plasma reagin test RPR-C Rapid plasma reagin card test RPR-S Sekure rapid plasma reagin test RU RPR units SCX Strong cation exchange SRM Selected reaction monitoring STD Sexually transmitted disease STI Sexually transmitted infection TaSP Treatment as prevention TOF Time of flight TPPA Treponema pallidum particle agglutination test TRUST Toludine Red Unheated Serum Test TT Treponemal test VDRL Venereal disease research laboratory test WHO World Health Organization WIV-ISP Scientific Institute of Public Health Belgium ⌘ 8 ⌘ Summary Syphilis, a multistage curable chronic disease caused by the spirochete Treponema pallidum ssp. pallidum (T. pallidum), has re-emerged during the last 15 years as a major global public health problem, with an estimated 6 million new infections each year worldwide. Men who have sex with men (MSM) populations have been particularly affected, accounting for more than 90% of incident syphilis infections in Belgium, whereby half of these are reinfections. If not treated promptly, syphilis can cause serious morbidity and adverse pregnancy events such as stillbirth and congenital defects. Epidemiological studies investigating the relationship between syphilis and HIV on different levels can yield insights into possible underlying determinants, such as sexual networK connectivity, that influence prevalence and incidence trends. Molecular phylogenetic approaches applied to sexually transmitted infection (STI) studies can also deepen our understanding of transmission dynamics. WorK presented in Section I of this thesis aimed to answer two important questions related to the relationship between syphilis and HIV. First, we assessed if there was a country-level association between antenatal syphilis prevalence from early in the HIV epidemics (1990-1999) and peak HIV prevalence. The purpose of this study was to help better elucidate the underlying determinants of variations in HIV spread. If evidence of a positive association would be found then this could be interpreted as evidence that the same underlying determinant(s) played a role in the spread of both HIV and syphilis and/or that syphilis was an important cofactor in the spread of HIV. Linear regression analyses of data from 76 countries revealed a strong association- syphilis prevalence in the 1990s predicted approximately 53% of the variation in peak HIV prevalence (chapter 2). Second, we assessed if we could use the HIV phylogenetic tree constructed from HIV-1 sequences of 1169 patients in follow- up at a single-centre cohort in Antwerp, Belgium to see if there was evidence for clustering of syphilis infections. We found no evidence of clustering, however, analyses revealed potential cases of sexual identity misclassification of MSM as heterosexuals. We discuss the role these individuals may play as a high-risk bridge population (chapter 3). Diagnosis of T. pallidum (re)-infection and post-treatment follow-up to determine pathogen eradication remains onerous for clinicians due to inadequate assays based on century-old techniques. Therefore, the development of a diagnostic test that could directly detect T. pallidum antigens in human biofluids such as blood and urine would represent considerable progress in improving individual care and prevention efforts. Mass spectrometry (MS)-based protein biomarker discovery methods may hold the Key to providing novel robust diagnostic targets. ⌘ 9 ⌘ Section II of this thesis details studies related to improving syphilis diagnostics by employing MS-based protein biomarker discovery techniques for antigen test development and a laboratory evaluation of an existent commercial nontreponemal syphilis assay. Since T. pallidum cannot be continuously cultured in vitro, bacteria were isolated from infected rabbits and purified to study the T. pallidum proteome during infection. Extracted proteins were trypsinized and subjected to multidimensional peptide separation and protein identification via matrix-assisted laser desorption ionization-time of flight (MALDI-TOF/TOF) and electrospray ionization (ESI-LTQ- Orbitrap) tandem mass spectrometry. These efforts resulted in the most extensive proteome investigation of T. pallidum to date; we were able to detect, characterize and semi-quantify
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