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Innovations in Rapid Mycoplasma Bovis INNOVATIONS IN RAPID MYCOPLASMA BOVIS DIAGNOSTICS WITH MALDI-TOF MS AND NANOPORE SEQUENCING Jade Bokma Dissertation submitted in fulfilment of the requirements for the degree of Doctor of Veterinary Sciences (PhD) 2021 Promoters: Prof. dr. B. Pardon Dr. F. Boyen Prof. dr. F. Haesebrouck Department of Large Animal Internal Medicine Department of Pathology, Bacteriology and Avian disease Faculty of Veterinary Medicine Ghent University Innovations in rapid Mycoplasma bovis diagnostics with MALDI-TOF MS and nanopore sequencing Innovaties in snelle Mycoplasma bovis-diagnostiek met MALDI-TOF MS en nanopore sequencing Jade Bokma Department of Large Animal Internal Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium Department of Pathology, Bacteriology and Avian disease, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium Cover: © Stan Jourquin and Creative Mania Printing: University Press Jade Bokma was supported by a doctoral grant (RF17/6313, MALDIRESP/MA) from the the Belgian Federal Public Service: Health, Food Chain Safety and Environment. “Perfection is achieved, not when there is nothing more to add, but when there is nothing left to take away” Antoine de Saint-Exupéry MEMBERS OF THE JURY Prof. dr. B. Pardon promoter Department of Large Animal Internal Medicine, Faculty of Veterinary Medicine, Merelbeke, Belgium Dr. F. Boyen promoter Department of Pathology, Bacteriology and Avian disease, Faculty of Veterinary Medicine, Merelbeke, Belgium Prof. dr. F. Haesebrouck promoter Department of Pathology, Bacteriology and Avian disease, Faculty of Veterinary Medicine, Merelbeke, Belgium Prof. dr. E. Claerebout head of the jury Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Merelbeke, Belgium Dr. F. Tardy UMR Mycoplasmoses des Ruminants, ANSES Laboratoire de Lyon, Lyon, France Dr. A. Heuvelink Royal GD, Animal Health, Deventer, The Netherlands Prof. dr. D. Maes Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Merelbeke, Belgium Prof. dr. S. Piepers M-team and Mastitis and Milk Quality Research Unit, Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Merelbeke, Belgium Dr. S. Theuns secretary Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Merelbeke, Belgium; Pathosense, Lier, Belgium. TABLE OF CONTENTS List of abbreviations 1 Preface 5 1 General introduction 7 1.1 Introduction on Mycoplasma bovis 9 1.2 Prevention and control 17 1.3 Antimicrobial and anti-inflammatory drug therapy 22 1.4 Identification of Mycoplasma bovis 29 1.5 Typing methods and diversity of Mycoplasma bovis 42 1.6 Antimicrobial susceptibility of Mycoplasma bovis 51 2 Scientific aims 101 3 Innovative methods for the identification of M. bovis 105 3.1 Non-specific, agar medium-related peaks can result in false positive Mycoplasma alkalescens and Mycoplasma arginini identification by MALDI-TOF MS 107 3.2 Optimizing identification of Mycoplasma bovis by MALDI-TOF MS 119 3.3 Rapid identification of Mycoplasma bovis from bovine bronchoalveolar lavage fluid with MALDI-TOF MS after enrichment procedure 131 3.4 Diagnostic test accuracy study on nanopore sequencing for the rapid identification of Mycoplasma bovis from individual and pooled bovine respiratory tract samples 157 4 Phylogenomic analysis of Mycoplasma bovis from Belgian veal, dairy, and beef herds 185 5 Antimicrobial susceptibility of Mycoplasma bovis 207 5.1 Antimicrobial susceptibility of M. bovis isolated from veal, dairy and beef herds 209 5.2 Genome -wide association study reveals genetic markers for antimicrobial resistance in Mycoplasma bovis 229 6 General discussion 255 6.1 Innovations in Mycoplasma bovis diagnostics 257 6.2 Mycoplasma bovis outbreak management 260 6.3 Use of Mycoplasma bovis diagnostics in purchase policy 268 6.4 Eradication or herd status certificates 271 6.5 Future prospects 274 Summary 281 Samenvatting 287 Curriculum Vitae 293 Bibliography 299 Dankwoord 307 LIST OF ABBREVIATIONS ADM Agar dilution method AID Anti-inflammatory drugs AFLP Amplification fragment length polymorphism AMR Antimicrobial resistance AMU Antimicrobial use AP-PCR Arbitrarily primed PCR AST Antimicrobial susceptibility testing BAL Bronchoalveolar lavages BALf Bronchoalveolar lavage fluid BLCM Bayesian latent class model BMD Broth microdilution BRD Bovine respiratory disease BTM Bulk tank milk BVDv Bovine viral diarrhea virus CBP Clinical breakpoint CCU Colour changing units CFU Colony forming units cgMLST Core genome MLST cgSNP Core genome single nucleotide variant CLSI Clinical and Laboratory Standards Institute COVID-19 SARS-CoV-2 DGGE Denaturing gradient gel electrophoresis DNS Deep nasal swab DOXY Doxycycline ECOFF Epidemiological cut-off ELISA Enzyme-linked immunosorbent assays ENRO Enrofloxacin EUCAST European Committee on Antimicrobial Susceptibility Testing FLOR Florfenicol GAM Gamithromycine GC Guanine-cytosine GEN Gentamicin 1 GWAS Genome-wide association study HRM High resolution melting curve analysis ICEs Integrative conjugative elements IHL In-house library IM Intramuscularly IS Insertion sequence ISM Iterative statistical method LR Likelihood ratio MALDI-TOF MS Matrix-assisted laser desorption-ionization – time of flight mass spectrometry MBT-ASTRA MALDI Biotyper-Antibiotic Susceptibility Test Rapid Assay Melt-MAMA Melt curve analysis of mismatch amplification mutation assays MIC Minimum inhibitory concentration MICEs Mycoplasma integrative conjugative elements MLST Multi-locus sequence typing MLVA Multiple-locus variable-number tandem repeat MPC Mutant prevention concentration MRSA Methicillin-resistant Staphylococcus aureus MSP Main spectra profiles MSW Mutant selection window NGS Next-generation sequencing NRI Normalized resistance interpretation NSAID Non-steroidal anti-inflammatory drugs nWT Non-wild type OIE World Organization for Animal Health ONT Oxford Nanopore Technologies/nanopore sequencing OXY Oxytetracycline PCR Polymerase chain reaction PFGE Pulsed-field gel electrophoresis PPLO Pleuropneumonia-like organisms PURE-LAMP Procedure for Ultra Rapid Extraction and Loop-mediated isothermal Amplification QRDR Quinolone resistance-determining region 2 RAPD Random amplification of polymorphic DNA RIMM Rapid identification of Mycoplasma bovis with MALDI-TOF MS SC Subcutaneously Se Sensitivity SMRT Single Molecule Real-Time SNP Single Nucleotide Polymorphism Sp Specificity ST Sequence type TIA Tiamulin TIL Tilmicosine TTA Transtracheal aspiration TTW Transtracheal washe TYL Tylosine UCC Unit changing color Vsps Variable surface lipoproteins wgMLST Whole genome MLST WGS Whole genome sequencing wgSNP Whole genome single nucleotide variant WHO World Health Organization WT Wild type 3 4 Preface PREFACE The recent viral pandemic in humans has made it clear to millions of people how crucial rapid diagnostics and applied biosecurity are in infectious disease control. Worldwide, cattle farmers and their veterinarians almost continuously face a similar challenge in their animals related to different and often simultaneous respiratory tract infections. Among these infections, Mycoplasma bovis is absolute priority. M. bovis is highly contagious and a leading indication for antimicrobial mass medication. Treatment is difficult as they are inherently resistant against many antimicrobials and can evade the immune response of the body facilitating chronic, persistent infections. Today, M. bovis control is still problematic. Effective biosecurity is hampered by incomplete epidemiological knowledge on M. bovis, especially concerning the existence of different strains and their spread between the dairy, beef and veal sector. Currently, using routine culturing, it takes more than a week to get a test result for M. bovis and susceptibility testing is not available. Alternative techniques like qPCR and antibody ELISA are often too expensive, lack sensitivity or show interpretative difficulties. Both for therapeutic outbreak management and more effective biosecurity, having rapid, accurate, and reasonably prized diagnostic tests available is crucial. Thriving on the technological evolution in the field of diagnostics, this doctoral thesis explores the possibilities of MALDI-TOF MS and nanopore sequencing to make M. bovis diagnosis more fast and reliable. Epidemiological results obtained by these new protocols were also incorporated, since prevention of spread is at least as essential as treatment to combat this resourceful pathogen. 5 6 Chapter 1 CHAPTER 1 GENERAL INTRODUCTION 7 8 General introduction Chapter 1 1.1 INTRODUCTION ON MYCOPLASMA BOVIS Characteristics of Mycoplasma species Mycoplasma bovis, previously known as Mycoplasma agalactiae var. bovis or M. bovimastitidis (Askaa and Erno, 1976), is one of the many known Mollicutes species (Razin, 1978). The class of the Mollicutes received its name due to the loss of their cell wall during evolution (molli: soft; cutis: skin) (Razin and Hayflick, 2010). More than 190 Mycoplasma species are currently documented (Rottem, 2003). These prokaryotes are among the smallest self-replicating organisms in the world (200-300 nm in diameter) (Razin, 1996), containing a genome length of 0.6-1 Mbp, with a low guanine-cytosine (GC) content of approximately 25- 30% (Thompson et al., 2011; Kumar et al., 2020). The genome length is very small, in comparison to other bacteria, such as Escherichia coli, of which the bacterial genome size
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