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1.2 Equine Periodontal Disease Kennedy, Rebekah Storm (2017) Microbiological and immunological aspects of equine periodontal disease. PhD thesis. https://theses.gla.ac.uk/8064/ Copyright and moral rights for this work are retained by the author A copy can be downloaded for personal non-commercial research or study, without prior permission or charge This work cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Enlighten: Theses https://theses.gla.ac.uk/ [email protected] Microbiological and immunological aspects of equine periodontal disease R.S. Kennedy BVMS (Hons) MRCVS Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy College of Medicine, Veterinary and Life Sciences University of Glasgow March 2017 © Rebekah Storm Kennedy, March 2017 Abstract Periodontal disease is a common and painful condition in the horse. Although awareness of the condition is growing amongst the veterinary profession and horse owners, the presence of the disease is often overlooked and treatment can be difficult. Despite this, there have been few recent studies of the aetiopathogenesis of the condition. Certain species of bacteria may act as periodontal pathogens, stimulating a destructive inflammatory response in periodontal tissues and this has been well recognised as being important to the aetiopathogenesis of the disease in man. However few equine studies on this aspect of the disease have been carried out. The main aims of this study were: - 1) to identify the bacteria associated with a healthy oral cavity and periodontitis in horses using culture dependent and independent methods; 2) to assess the differences in bacterial populations between the healthy and periodontitis groups and identify putative pathogens; 3) to quantify the expression patterns of TLRs 2, 4 and 9, the pro-inflammatory cytokines IL-1β and TNFα, anti- inflammatory cytokine IL-10 and Th1/Th2/Th17 cytokines IL-4, IL-6/ IL-12, IFNɣ/ IL-17, within gingival tissue from each sample group; 4) to use matched data to establish if associations exist between the presence and quantity of bacterial species present and TLR expression and 5) to determine activation of TLRs 2, 4 and 9 by putative pathogens using specific in- vitro TLR assays. Swabs were taken from the gingival sulcus of 42 orally healthy horses and plaque samples were taken from the periodontal pockets of 61 horses with periodontal disease. The location and grade of the lesion was noted and an equine dental chart completed for each case. Bacteria were identified using high throughput 16S rRNA gene sequencing, QPCR, whole genome sequencing and conventional culture followed by 16S gene sequencing. Gingival biopsies were taken from 13 orally healthy horses and 20 horses with periodontitis and gene expression of TLR 2, TLR 4, TLR 9, IL-1β, IL-4, IL-6, IL-10, IL-12, IL-17, TNFα and IFNɣ was measured. THP-1X Blue, MyD88 THP-1X Blue, HEK hTLR 2 Blue and HEK hTLR 4 Blue human cell lines were co-cultured with putative periodontal pathogens and their response measured via level of secreted embryonic alkaline phosphatase. Clinical, microbiological and immunological data underwent cross-matching analysis. i Microbial populations showed 89% dissimilarly between oral health and periodontitis with a less diverse population present in diseased equine periodontal pockets. The most discriminative bacteria between health and disease identified at genus level were Fusobacteria and Acinetobacter in health and Pseudomonas and Prevotella in periodontitis. The most abundant genera were Gemella (36.5%), Pseudomonas (14%) and Acinetobacter (8%) in orally healthy samples and Pseudomonas (25%), Prevotella (14%) and Acinetobacter (9.4%) in periodontitis samples. Whole genome sequencing revealed the presence of 75 species of Prevotella in the equine oral cavity and a significantly higher number of reads corresponding to Prevotella bivia, Prevotella dentalis, Prevotella denticola, Prevotella intermedia, Prevotella melaninogenica, Prevotella nigrescens were noted in diseased samples. Significant increases in expression of TLR 4 mRNA, TLR 9 mRNA and, in particular TLR 2, mRNA were noted in diseased equine gingival tissue in addition to increased pro- inflammatory and anti-inflammatory cytokine mRNA expression. Presence of P. intermedia was significantly positively correlated with expression of TLR 2 in equine periodontitis. In addition, the presence of Aggregatibacter actinomycetemcomitans was positively associated with disease severity and expression of TLR 4 mRNA in the horse. Co-culture of periodontal pathogens with human cell lines revealed that the innate immune response to the presence of these bacteria is mainly mediated through TLR 2 activation. The use of both culture dependent and culture independent methods to investigate the equine oral microbiome has provided significant breadth and depth of information on the microbiology of equine periodontal disease. Microbial populations are significantly different as expected and bacteria belonging to the Prevotella genus have been strongly implicated in the aetiopathogenesis of the condition. The innate immune response produced in periodontally diseased equine gingival tissue has been characterised for the first time in the horse. ii Table of Contents Abstract ....................................................................................... i Table of Contents .......................................................................... iii List of tables ................................................................................ vi List of figures .............................................................................. vii Acknowledgements .......................................................................... x Declaration .................................................................................. xi Abbreviations .............................................................................. xii Chapter 1 Introduction .................................................................... 1 1.1 Equine dental anatomy and physiology ....................................... 3 1.1.1 The Equine oral cavity ...................................................... 3 1.1.2 The equine periodontium................................................... 7 1.2 Equine periodontal disease ..................................................... 9 1.2.1 Clinical signs.................................................................. 9 1.2.2 Prevalence ................................................................... 10 1.2.3 Aetiopathogenesis .......................................................... 11 1.2.4 Diagnosis and staging of equine periodontal disease .................. 20 1.2.5 Treatment and management .............................................. 22 1.3 Equine oral microbiology ....................................................... 24 1.3.1 Bacteria in the oral cavity ................................................. 24 1.3.2 The equine oral microbiome .............................................. 27 1.4 Innate immunity in the oral cavity ............................................ 33 1.4.1 The innate immune response ............................................. 33 1.5 Summary .......................................................................... 53 1.6 Aims and objectives ............................................................. 54 Chapter 2 General materials and methods ............................................ 55 2.1 Ethical approval ................................................................. 55 2.2 Sample population ............................................................... 55 2.2.1 Sample collection ........................................................... 55 2.2.2 Sample processing .......................................................... 57 2.3 Individual studies ................................................................ 63 2.4 Statistical analysis ............................................................... 63 2.5 List of suppliers .................................................................. 64 2.6 General stock solutions and buffers .......................................... 66 Chapter 3 Equine dental examination .................................................. 67 3.1 Introduction ...................................................................... 67 3.2 Materials and methods .......................................................... 69 iii 3.2.1 Signalment ................................................................... 69 3.2.2 Oral and clinical examination ............................................. 69 3.2.3 Statistical analysis .......................................................... 72 3.3 Results ............................................................................ 72 3.3.1 Study population ............................................................ 72 3.3.2 Signalment ................................................................... 73 3.3.3 Clinical examination ....................................................... 80 3.4 Discussion ......................................................................... 85 3.5 Conclusion .......................................................................
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