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The Ecology and Epidemiology of Rickettsia Felis in Australia Yen

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The Ecology and Epidemiology of Rickettsia Felis in Australia Yen The ecology and epidemiology of Rickettsia felis in Australia Yen Thon Teoh ORCID identifier: 0000-0003-1836-8762 This thesis is being submitted for total fulfillment of a Doctor of Philosophy November, 2018 FACULTY OF VETERINARY AND AGRICULTURAL SCIENCES THE UNIVERSITYOF MELBOURNE,VICTORIA,AUSTRALIA ABSTRACT ABSTRACT Rickettsia felis is an emerging flea-borne zoonosis that is being increasingly recognised to contribute to unspecified malaise often referred to as fevers of unknown origins. The cat flea, Ctenocephalides felis, has been most widely accepted as the biological vector for R. felis. It is an adaptable ectoparasite that readily feeds on companion animals and opportunistically on other mammalian hosts. Its ability to persist in environments and on pets despite challenges from grooming, cleaning and prophylactic medications has led to the development of innumerable commercial preventatives designed to protect against infestation. The cat flea and its endosymbiont, R. felis, have managed to disseminate along with its canine and feline hosts across continents, presenting a potential risk to human health, Australia being of no exception. Despite the widespread presence of the cat flea and its promiscuous host-feeding behaviour, the contribution of R. felis to human morbidity, resulting loss of productivity and reduced quality of life in Australia remains largely unknown. Moreover, demographic, ecological and climatic risk factors for R. felis in Australia remain uninvestigated. This study sets out the foundation to address these knowledge gaps in Australia by i) retrospec- tively testing sera of patients previously testing positive for murine typhus for R. felis exposure; ii) determining the prevalence and associated demographic, occupational and geographical risk factors contributing to R. felis exposure in Australian veterinarians and; iii) determining the role of rodents as peri-domestic reservoirs for R. felis, and; iv) determining the geographical and climatic risks contributing to R. felis infestation rates in cat fleas in eastern coastal Australia. Historically, a specific diagnosis of flea-borne spotted fever (FBSF) was limited, owing to im- munogenic cross-reactivity with Rickettsia typhi. Thus patients who had been exposed to R. felis were not able to be specifically tested. Of 49 patient sera previously testing antibody positive for murine typhus at the Australian Rickettsial Reference Laboratory, Geelong, 14 patients yielded specific antibodies to R. felis, seven yielded specific antibodies to R. typhi, while 28 patients were classified as indeterminate (with titres reacting between two-fold across the two organisms). Of R. felis positive patients, 5 demonstrated seroconversion, indicating a recent infection that was likely contributing to clinical signs observed by their referring doctor. Despite a cluster of ii five individual FBSF cases being reported for the first time in Australia in 2009, it is clear that other FBSF cases have remained undiagnosed or misdiagnosed, advocating the need for medical practitioners to obtain relevant history on patient’s exposure to domestic pets and their fleas. The second study sought to address the prevalence and associated risk factors for R. felis ex- posure in a high-occupational risk group, veterinarians. Of 131 veterinarians tested across Australia, 16.0% were found specifically seroreactive to R. felis. Older veterinarians were signif- icantly protected from exposure (OR 0.752, p 0.04, 95% CI 0.579 0.975), as were those Æ Æ Æ ¡ that recommended flea treatment to their clients(OR 0.611, p 0.044, 95% CI 0.38 0.982). Æ Æ Æ ¡ Surprisingly, participants from the cooler south-eastern states of Victoria and Tasmania were trending toward a higher odds of exposure compared with other, warmer states (OR 1.381, Æ p 0.075, 95% CI = 0.973 1.96). This was at odds with preconceptions on the ecology of Æ ¡ ectoparasites; warmer subtropical and tropical regions were associated with higher environmen- tal flea burdens. Moreover, this study demonstrated the high degree of exposure of R. felis in veterinarians, suggesting incidence of FBSF may be underrepresented in Australia. For the third study, fleas collected from client-owned dogs and cats in different climatic zones along the east coast of Australia were screened for R. felis, to determine infection rates of R. felis URRWXCal2 in C. felis felis. Infection rates of 6.7%, 13.2% and 15.5% were obtained by real-time PCR (qPCR) in tropical, subtropical and temperate regions, respectively. Univariate analysis indicated that fleas from toy/small breed dogs were less likely to be harbouring R. felis (p 0.033), as were Domestic Medium Hair (DMH) and pedigree-breed cats (p 0.0002 Æ Æ and p 0.043 respectively). Cooler minimum temperature ranges of between 15 to 20°C and Æ between 8 to 15°C increased the odds of R. felis positivity in fleas, as did a constrained maximum temperature range of between 27 to 30°C on multivariable analysis. In conclusion this study demonstrated that environmental conditions such as temperature play a part in influencing R. felis survival and infectivity within its flea host, which suggests that public health risk mitigation measures need to consider regional differences to adequately comprehend transmission risk of flea-borne spotted fever. Finally, the involvement of peri-domestic animals in the life cycle of R. felis was investigated. Within urban environments, movement of companion animals is limited by legislation and animal control initiatives. Rodents are able host the cat flea vector, but their participation in iii ABSTRACT perpetuating the life cycle of R. felis hasn’t been conclusively demonstrated. Brain and spleen tissue collected from 256 native and introduced rats (Rattus fuscipes, Rattus norvegicus and Rattus rattus)in south-east Queensland were tested for rickettsiae by qPCR, with none detectably positive, suggesting that they do not play a significant part in maintaining R. felis. This series of studies represents an in-depth look at the ecology of R. felis in Australia, and provides an insight into characteristics that makes it such a successful but often overlooked organism. Awareness amongst the public, medical practitioners and veterinarians is currently poorly developed, and diagnosis of the condition has suffered as a result. iv DECLARATION The thesis comprises only original work from the candidate towards the Doctor of Philosophy degree except where due reference has been indicated in the preface. Due acknowledgement has been made in the text for to all other material used. Contributions by others to jointly-authored works have been clearly stated and includes the following: • Study conception and design • Statistical data analysis • Survey design • Laboratory technical assistance • Validation of experimental results • Professional editorial advice Portions of the thesis that have been previously submitted to qualify for the award of any other degree or diploma at any university or tertiary institution, if any, have been clearly stated. The thesis is fewer than the maximum word limit in length exclusive of tables, maps, bibliogra- phies and appendices. Signed: Yen Thon Teoh v PREFACE PREFACE The following is a description of the work towards the thesis that was carried out by the author in collaboration with others, with the nature and proportion of the work done by each contributor indicated. Publications during candidature Peer-reviewed papers Teoh, Y. T., Hii, S. F.,Graves, S., Rees, R., Stenos, J., & Traub, R. J. (2016). Evidence of exposure to Rickettsia felis in Australian patients. One Health, 2, 95-98. Name Role Contribution Yen Thon Teoh1 Acquisition of data 100% Analysis and interpretation of data 60% Drafting the manuscript 100% Sze Fui Hii Analysis and interpretation of data 5% Revising the article critically 20% Stephen Graves Analysis and interpretation of data 15% Revising the article critically 20% Robert Rees Study design 33% Revising the article critically 10% John Stenos Study design 33% Analysis and interpretation of data 15% Revising the article critically 25% Rebecca Traub Study design 34% Analysis and interpretation of data 5% Revising the article critically 25% 1Candidate vi Teoh, Y. T., Hii, S. F., Stevenson, M. A., Graves, S., Rees, R., Stenos, J., & Traub, R. J. (2017). Serological evidence of exposure to Rickettsia felis and Rickettsia typhi in Australian veterinarians. Parasites & vectors, 10(1), 129. Name Role Contribution Yen Thon Teoh1 Study design 30% Acquisition of data 100% Analysis and interpretation of data 60% Drafting the manuscript 100% Sze Fui Hii Analysis and interpretation of data 5% Revising the article critically 20% Mark Stevenson Analysis and interpretation of data 20% Stephen Graves Revising the article critically 20% Robert Rees Study design 20% Revising the article critically 10% John Stenos Study design 20% Analysis and interpretation of data 5% Revising the article critically 25% Rebecca Traub Study design 30% Analysis and interpretation of data 10% Revising the article critically 25% Teoh, Y. T., Hii, S. F., Graves, S., Rees, R., Stenos, J., & Traub, R. J. (2018). The epidemiology of Rickettsia felis infecting fleas of companion animals in eastern Australia. Parasites & Vectors 11(1), 138. Name Role Contribution Yen Thon Teoh1 Study design 10% Acquisition of data 80% Analysis and interpretation of data 80% Drafting the manuscript 100% continued.. 1Candidate vii PREFACE Name Role Contribution Sze Fui Hii Study design 10% Analysis and interpretation of data 5% Revising
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