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Molecular Characterisation of Selected Enteric Pathogens and Antimicrobial Resistance of Salmonella in Rangeland Goats in Wester

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Molecular Characterisation of Selected Enteric Pathogens and Antimicrobial Resistance of Salmonella in Rangeland Goats in Wester Molecular characterisation of selected enteric pathogens and antimicrobial resistance of Salmonella in rangeland goats in Western Australia Thesis presented by Khalid Rasheed Saif Al-Habsi BSc, MScAnSc for the degree of Doctor of Philosophy School of Veterinary and Life Sciences Murdoch University 2017 Declaration I declare that this thesis is my own account of my research and contains as its main content work, which has not been previously submitted for a degree at any tertiary education institution. The methods and results described in this thesis reflect the work performed and are supported with records in the lab books. Khalid Rasheed Saif Al-Habsi December 2017 i Statement of Contribution The five experimental chapters presented in this thesis have been either published as peer reviewed articles (Chapters 3-6) or submitted (Chapter 9) with multiple co- authors. Khalid Rasheed Saif Al-Habsi was the first author on these publications, primarily involved in conceiving ideas and project design, laboratory work, data analysis, interpretation of results and preparation of manuscripts. All publication co-authors have consented to their work being included in this thesis and have accepted this statement of contribution. Chapter Title Contribution 3 Zoonotic Cryptosporidium and Giardia K Al-Habsi: 80 % shedding by captured rangeland goats C Jacobson: 8 % U Ryan: 5 % R Yang: 3 % D Miller: 3% A Williams: 1% 4 Morphological and molecular K Al-Habsi: 76 % characterization of three Eimeria species C Jacobson: 11% from captured rangeland goats in western U Ryan: 9 % Australia R Yang: 3 % D Miller: 1% 5 Morphological and molecular K Al-Habsi: 78 % characterization of an uninucleated cyst- U Ryan: 16 % producing Entamoeba spp. in captured R Yang: 3 % rangeland goats in western Australia D Miller 2% C Jacobson: 1 % 6 Molecular characterisation of Salmonella K Al-Habsi: 71 % enterica serovar Typhimurium and C Jacobson: 16 % Campylobacter jejuni faecal carriage by U Ryan: 6 % captured rangeland goats S Abraham: 2% R Yang: 3% D Miller: 2% 9 Salmonella enterica isolates from K Al-Habsi: 83 % Western Australian rangeland goats D Jordan: 5% remain susceptible to critically important S Abraham: 3% antimicrobials A Harb: 2% T Laird: 2% R Yang: 2% C Jacobson: 1% U Ryan: 1% D Miller: 1% ii Abstract The Australian goat meat industry is largely supported by the sale of captured feral goats derived from rangeland production systems. Diarrhoea and ill-thrift following capture is a major issue for the industry, yet relatively little is known about the role of infectious disease and the public health significance of gastrointestinal infections. The aim of this thesis was to characterise faecal carriage of selected enteric pathogens by rangeland goats using molecular tools, and to determine potential impacts for goat productivity and public health. A longitudinal study conducted using qPCR and sequencing to screen faecal samples revealed that faecal carriage (prevalence) and shedding intensity of enteric pathogens were generally highest on arrival at the goat depot (feedlot), immediately after capture and transport. Three Cryptosporidium species (C. xiaoi, C. ubiquitum and C. parvum), Giardia duodenalis Assemblage E, three Eimeria species (E. ahsata, E. crandallis and E. arloingi), E. bovis-like Entamoeba sp., Salmonella enterica serovar Typhimurium, Campylobacter jejuni, Haemonchus contortus and Trichostrongylus spp. were identified in faecal samples from the rangeland goats using molecular tools. Of these, C. ubiquitum subtype XIIa, C. parvum subtypes IIaA17G2R1 and IIaA17G4R1, G. duodenalis Assemblage E, S. enterica serovar Typhimurium and C. jejuni are considered zoonotic or emerging zoonotic pathogens. These studies provided the first description of caprine Eimeria cytochrome c oxidase subunit I (COI) and Entamoeba bovis-like actin sequences, and successfully produced a longer (1,229 bp) 18S rRNA sequence of E. arloingi. Of the pathogens identified in faecal samples, only Cryptosporidium was associated with an increased risk of scouring (diarrhoea) and reduced growth in the following one-month period. Giardia faecal carriage and higher Eimeria oocyst counts were associated with looser faecal consistency, but not to the point where scouring risk was increased. iii A subsequent investigation of rangeland goats consigned from four locations identified high rates (23-30%) Salmonella faecal carriage, with three serovars identified (S. Typhimurium, S. Chester and S. Saintpaul) at slaughter, indicating the potential for downstream carcass contamination and food safety concerns. A high percentage of Salmonella isolates (84.0%) remained entirely susceptible to all antimicrobials tested, which is encouraging, with low rates (4/106) of multi-drug resistance (resistant to three of more classes of antimicrobials) and no resistance to critically important antimicrobials (fluoroquinolones and third generation cephalosporins) was observed. The findings of the present study have important implications for management and animal welfare of captured rangeland goats starting from capture yards and feedlots through to slaughter to reduce public health risks. iv Table of Contents Declaration .................................................................................................................... i Statement of Contribution ............................................................................................ ii Abstract ....................................................................................................................... iii List of Figures ........................................................................................................... xiv List of Tables ............................................................................................................. xvi Acknowledgements ................................................................................................... xix Publications arising from this thesis ......................................................................... xxii Poster presentations of work contained within this thesis ....................................... xxiv Symbols and Abbreviations ...................................................................................... xxv CHAPTER 1. LITERATURE REVIEW ............................................................... 29 1.1. Introduction .................................................................................................. 29 1.2. Cryptosporidium........................................................................................... 29 1.2.1. Taxonomy of Cryptosporidium .................................................................... 30 1.2.2. Life cycle of Cryptosporidium ..................................................................... 33 1.2.3. Prevalence of Cryptosporidium in goats ...................................................... 35 1.2.4. Host immune response to Cryptosporidium ................................................. 36 1.2.5. Pathogenesis of Cryptosporidium ................................................................ 36 1.2.6. Diagnosis of Cryptosporidium ..................................................................... 37 1.2.7. Treatment of Cryptosporidiosis .................................................................... 37 1.3. Giardia ......................................................................................................... 38 1.3.1. Life cycle of Giardia .................................................................................... 42 1.3.2. Prevalence of Giardia in livestock and goats............................................... 43 1.3.3. Pathogenesis of Giardia ............................................................................... 44 1.3.4. Host immune response to Giardia ............................................................... 44 1.3.5. Diagnosis of Giardia .................................................................................... 44 1.3.6. Treatment of Giardia ................................................................................... 45 v 1.4. Eimeria ......................................................................................................... 45 1.4.1. Taxonomy of Eimeria .................................................................................. 46 1.4.2. Life cycle of Eimeria.................................................................................... 48 1.4.3. Prevalence of Eimeria in goats..................................................................... 50 1.4.4. Pathogenesis of Eimeria in goats ................................................................. 50 1.4.5. Host immune response to Eimeria ............................................................... 51 1.4.6. Diagnosis of coccidiosis ............................................................................... 51 1.4.7. Treatment of Eimeria ................................................................................... 51 1.5. Entamoeba .................................................................................................... 52 1.5.1. Prevalence of Entamoeba ............................................................................. 52 1.5.2. Pathogenesis and host immune response to Entamoeba .............................. 53 1.5.3. Diagnosis of Entamoeba .............................................................................. 53 1.5.4. Treatment of Entamoeba .............................................................................
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