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Detection and Epidemiology of Coxiella Burnetii Infection in Beef Cattle in Northern Australia and the Potential Risk to Public Health

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Detection and Epidemiology of Coxiella Burnetii Infection in Beef Cattle in Northern Australia and the Potential Risk to Public Health Detection and epidemiology of Coxiella burnetii infection in beef cattle in northern Australia and the potential risk to public health Caitlin Medhbh Wood BVSc (Hons1) MANZCVS (Veterinary Epidemiology) https://orcid.org/0000-0003-2716-0402 A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2020 School of Veterinary Science Abstract Q fever has a longstanding history in Queensland, Australia. Although it is not a new disease to Australia, Q fever continues to burden the country with some of the highest annual case notification rates globally (Tozer 2015). While there are undeniable links with Q fever cases and exposure to cattle, it appears that coxiellosis predominantly goes undiagnosed and unnoticed in cattle within Australia. Knowledge of the prevalence and distribution of coxiellosis in cattle populations across northern Australia is limited due to minimal surveillance and no standardisation of diagnostic test methods. The overall aim of this PhD project was to improve the understanding of the epidemiology of coxiellosis in beef cattle in northern Australia and gain insights into the potential risk to public health. Descriptive analyses of 2,838 human Q fever notifications from Queensland between 2003 and 2017 were initially reported. Queensland accounted for 43% of the Australian national Q fever notifications for this period. From 2013–2017 the most common identifiable occupational group was agricultural/farming. For the same period, at-risk environmental exposures were identified in 82% (961/1,170) of notifications; at-risk animal-related exposures were identified in 52% (612/1,170) of notifications; abattoir exposure was identified in 7% of notifications. Improved surveillance since 2012 has highlighted the need for further education and heightened awareness of Q fever risk for all people living in Queensland, not just those in previously considered high-risk occupations. A focused molecular survey was conducted at an abattoir in Queensland aimed to: 1) estimate the prevalence of C. burnetii infection in a population of beef cattle going to slaughter, and 2) enable identification of specific genotypes of C. burnetii infecting cattle in this population. Cattle originating from several Queensland regions and northern New South Wales had reproductive tissue and liver tissue collected for molecular testing. C. burnetii DNA was detected, although at a lower than expected frequency, from the liver of cattle originating from Darling Downs South West, Central Queensland and North Queensland regions. No evidence of C. burnetii infection was detected in placental tissue or amniotic fluid samples from pregnant cattle post-mortem during this study. During the next study, a human indirect immunofluorescence assay (IFA) was modified and validated for the detection of IgG antibodies against phase I and/or phase II C. burnetii in bovine sera and determined an optimal screening dilution cut-off to be 1:160. Direct comparison of the modified IFA with the commercial IDEXX enzyme-linked immunosorbent assay (ELISA) i kit (Q Fever Ab Test IDEXX Laboratories, United States of America) was performed by testing 458 serum samples from four distinct cattle populations across the east coast of Australia and New Zealand. Results were then analysed using Bayesian latent class modelling, to validate the tests in the absence of a gold standard reference test. This analysis indicated that the IFA had an estimated diagnostic sensitivity (DSe) of 73.6% (95% Credible Interval (CrI) 61.1–85.9) and diagnostic specificity of (DSp) 98.2% (95%CrI 95.1–99.7). The commercial IDEXX ELISA kit was found to have a higher DSe of 87.9% (95%CrI 73.9–96.4) and similar DSp of 97.7% (95%CrI 93.2–99.7). The IFA was used to test 2,012 sera samples from beef cattle managed on commercial properties located in Queensland and the Northern Territory. Bayesian latent class models were then developed to estimate the true prevalence of exposure, adjusted for diagnostic test sensitivity and specificity and incorporating the hierarchical structure of the cattle within properties and regions. In this study, cattle in the Northern Territory had lower estimated true prevalence than cattle within most regions of Queensland with the exception of south-east Queensland. Results from this study have provided baseline true prevalence estimates and described the geographic distribution of C. burnetii exposure in a sample of extensively managed beef cattle located across the tropical grazing regions of northern Australia. Finally, C. burnetii IFA results from the previous chapter and additional molecular testing of vaginal swab samples from the same sample of cattle were examined to investigate the relationship between coxiellosis and reduced reproductive performance in beef cattle. A large dataset investigating causes of reduced reproductive performance in beef cattle across northern Australia was analysed and results indicated that high levels of C. burnetii exposure on properties was associated with reduced pregnancy rates, although further research is needed to confirm this hypothesis. This thesis has explored several aspects of Q fever in humans and coxiellosis in beef cattle from the northern Australian context. Laboratory and epidemiological research outcomes have provided tools for improved surveillance in cattle and has improved our understanding of potential public health risks. In Australia, current Q fever control practices are isolated to human vaccination without any surveillance, control programs nor licensed vaccines in animals. Further research in livestock and wildlife will further improve our ability to control Q fever and manage health and productivity within agricultural industries. ii Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, financial support and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my higher degree by research candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co- authors for any jointly authored works included in the thesis. iii Publications included in this thesis Tozer S, Wood C, Si D, Nissen M, Sloots T, Lambert S. (2020) The improving state of Q fever surveillance: A review of Queensland notifications, 2003–2017, Communicable Diseases Intelligence, Vol. 44; pp 1-22 Wood C, Tan T, Muleme M, Barnes T, Bosward K, Alawneh J, McGowan M, Stenos J, Gibson J, Perkins N, Firestone S, Tozer S. (2019) Validation of an indirect immunofluorescence assay for the detection of IgG antibodies against Coxiella burnetii in bovine serum, Preventive Veterinary Medicine, Vol. 169; article number 104698 Wood C, Perkins N, Tozer S.J, Johnson W, Barnes T, McGowan M, Gibson J, Alawneh J, Perkins N, Firestone S, Woldeyohannes S. (2021) Prevalence and spatial distribution of Coxiella burnetii seropositivity in northern Australian beef cattle adjusted for diagnostic test uncertainty, Preventive Veterinary Medicine, 189: 105282 Other publications during candidature Clark N.J, Tozer S, Wood C, Firestone S.F, Stevenson M, Caraguel C, Chaber A-L, Heller J, Soares Magalhães R.J. (2020) Unravelling animal exposure profiles of human Q fever cases in Queensland, Australia using natural language processing, Transboundary and Emerging Diseases, Vol. 67, Issue 5; pp 2133 - 2145 Oral presentations Wood C, Tozer S, Gibson J, Alawneh J, McGowan M, Perkins N, Prevalence and spatial distribution of Coxiella burnetii exposure in beef cattle across northern Australia, Meat and Livestock Australia Postgraduate Conference, Q Station, Sydney, November 2018 Wood C, Seroprevalence of Coxiella burnetii in north Australian beef cattle using an indirect immunofluorescence assay, Australian and New Zealand College of Veterinary Scientists (ANZCVS) Science Week 2018, Epidemiology Chapter Conference Proceedings, July 2018 Wood C, Seroprevalence of Coxiella burnetii in north Australian beef cattle using an indirect immunofluorescence assay, Australian and New Zealand College of Veterinary Scientists (ANZCVS) Science Week 2018, Cattle Chapter Conference Proceedings (invited speaker), July 2018 iv Wood C, Tan T, Muleme M, Barnes T, Bosward K, Alawneh J, McGowan
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