Investigations Into the Epidemiological and Clinical Effects of Bovine Viral Diarrhoea Virus Infection in Sheep and Other Non-Bovine Species in Australia
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Investigations into the epidemiological and clinical effects of bovine viral diarrhoea virus infection in sheep and other non-bovine species in Australia by Caitlin Alexandra Evans BSc. Honours (University of Adelaide) A thesis submitted to the University of Adelaide in fulfilment of the requirements for the degree of Doctor of Philosophy School of Animal and Veterinary Sciences Roseworthy Campus The University of Adelaide 2017 Table of Contents Abstract ....................................................................................................................................... 6 Declaration of Originality ........................................................................................................... 8 Acknowledgments ...................................................................................................................... 9 Chapter 1: An introduction to ruminant pestiviruses ................................................................ 10 1.1 Pestivirus diversity ................................................................................................. 10 Bovine viral diarrhoea virus .............................................................................. 11 Border Disease virus .......................................................................................... 11 Biotypes .............................................................................................................. 12 1.2 Outcomes of infection ............................................................................................ 13 Acute Infections .................................................................................................. 13 Foetal Infection .................................................................................................. 14 Persistent Infection ............................................................................................. 16 1.3 Economic Cost ....................................................................................................... 17 Bovine viral diarrhoea virus .............................................................................. 17 Border disease virus ........................................................................................... 18 1.4 Diagnosis ................................................................................................................ 18 Antibody testing .................................................................................................. 18 Virus or virus-specific antigen testing ................................................................ 20 1.5 Control and eradication .......................................................................................... 23 Preventing infection of susceptible animals ....................................................... 23 Identifying and eliminating persistently infected animals .................................. 24 Risks to Pestivirus control .................................................................................. 25 2 1.6 Cross species transmission ..................................................................................... 27 Bovine viral diarrhoea virus .............................................................................. 27 Border disease virus ........................................................................................... 30 1.7 History of ruminant pestiviruses in Australia ........................................................ 32 Prevalence .......................................................................................................... 33 1.8 Thesis outline ......................................................................................................... 37 Chapter 2: Diagnosis of BVDV-specific antibodies in sheep serum ........................................ 40 2.1 Identifying BVDV-1specific antibodies in sheep serum ....................................... 41 Original article: Investigation of AGID and two commercial ELISAs for the detection of Bovine viral diarrhea virus-specific antibodies in sheep serum .... 42 2.2 Chapter discussion ................................................................................................. 49 Chapter 3: Outcomes of acute BVDV-1c infections in pregnant ewes .................................... 51 3.1 Findings in ewes..................................................................................................... 53 Original article: Clinical responses and reproductive outcomes in pregnant ewes experimentally infected with bovine viral diarrhoea virus (Type-1c) between days 59 and 69 of gestation .................................................................. 54 3.2 Findings in lambs ................................................................................................... 64 Original article: Pathological outcomes in lambs born to ewes experimentally infected with bovine viral diarrhea virus Type-1c (BVDV-1c) between 59 and 69 days of gestation ................................................................................................. 65 3.3 Chapter discussion ................................................................................................. 93 Chapter 4: Transmission of BVDV-1c in sheep ....................................................................... 96 4.1 Transmission from persistently infected sheep ...................................................... 98 3 Original article: Natural transmission of BVDV-1c from a persistently infected, neonate lamb to naïve sheep and cattle .............................................................. 99 4.2 Transmission from acutely infected sheep ........................................................... 119 Short communication: The risk of transmission from sheep experimentally infected with BVDV-1c during the acute phase to BVDV naïve sheep ............. 120 4.3 Chapter discussion ............................................................................................... 127 Chapter 5: Acute BVDV-1c infections in alpacas .................................................................. 130 5.1 Findings in alpacas ............................................................................................... 131 Original article: BVDV in Australian alpacas: Natural infection and clinical profiles following co-mingling with a persistently infected heifer ................... 132 5.2 Chapter discussion ............................................................................................... 158 Chapter 6: Prevalence of antibodies to Pestiviruses in Australian sheep and other livestock species ..................................................................................................................................... 160 6.1 Prevalence of antibodies to Pestiviruses in sheep ................................................ 162 Short communication: Seroprevalence of antibodies to Pestivirus infections in South Australian sheep flocks ........................................................................... 163 6.2 Prevalence of antibodies to Pestiviruses in other livestock species ..................... 175 Original article: Antibodies to bovine viral diarrhoea virus (BVDV) in water buffalo (Bubalus bubalis) and cattle from the Northern Territory of Australia176 6.3 Chapter discussion ............................................................................................... 182 Chapter 7: Discussion and Conclusions.................................................................................. 184 Appendix 1: Supporting Publications – Published papers ...................................................... 190 4 Original article: Reproductive performance in experimentally BVDV infected ewes and seroconversion rates in sheep co-mingled with BVDV PI calves ..... 191 Appendix 2: Supporting Publications – Conference papers ................................................... 198 Oral Conference Presentations ................................................................................... 199 Poster Conference Presentations ................................................................................ 200 References ............................................................................................................................... 201 5 Abstract Bovine viral diarrhoea is a disease of cattle known to cause severe reproductive dysfunction and immunosuppression in infected animals. It has also been reported that the BVD virus (BVDV) is able to cross species barriers infecting non-bovine species such as sheep, goats, deer and alpacas. The ability of BVDV to infect species other than cattle is of great concern when developing control or eradication programs for BVDV, particularly in areas where cattle regularly come into contact with other susceptible species. As such, the main objective of this thesis was to investigate the epidemiological and clinical effects associated with BVDV infections in sheep and other commonly farmed Australian livestock species. Firstly, the clinical and reproductive outcomes following acute infections of pregnant ewes was studied. Twenty two ewes were experimentally infected with BVDV-1c between 59 to 69 days of gestation and the clinical and reproductive outcomes of these ewes were compared to those of a control group of 11 BVDV naïve and uninfected ewes. In the naïve ewe flock a lambing rate of 172.7% was recorded, lambs were born clinically normal and had a high