Epidemiology and Transmission of Theileria orientalis in Australasia.

Oriental theileriosis, a disease primarily impacting cattle is caused by an apicomplexan hemoprotozoan parasite, Theileria orientalis. It has now become established in the Australasia region. The organism was long considered a benign cause of persistent infections; however, an increase in clinical outbreaks since 2006 in the eastern Australian states and New Zealand was associated with the identification of the pathogenic Ikeda (Type 2) and Chitose (Type 1) genotypes. Unlike the pathogenic T. parva and T. annulate, which target leucocytes, clinical manifestation with T. orientalis is due to its effects on erythrocytes, with the infection sometimes designated as Theileria associated bovine anemia (TABA). In Australia and New Zealand, the tick Haemaphysalis longicornis is the principal vector, though other Haemaphysalis species are also likely vectors. The endemic status of infection with pathogenic genotypes in areas with low or absent tick populations is an apparent paradox that may be attributable to alternative modes of transmission, such as mechanical transmission by hematophagous insects (lice, mosquitoes, and biting flies), vertical transmission, and transmission via iatrogenic means. This review addresses the evidence for the different modes of transmission of T. orientalis with particular focus on the reported and potential vectors in Australasia.

Detection and distribution of haematophagous flies and lice on cattle farms and potential role in the transmission of Theileria orientalis.

On the Northern Tablelands of New South Wales, Australia, endemic Theileria orientalis infection of cattle has been reported on farms where no ticks have been observed, raising the question of how Theileria is transmitted in these areas. To investigate the potential role of mechanical transmission by insects, the present study investigated the seasonal dynamics of biting fly species trapped between December 2017 and May 2019 on six cattle farms in the region where the presence of Theileria was confirmed. These flies, sucking lice collected from these farms and pools of Culicoides species affecting cattle also trapped in the region were subjected to qPCR detection of T. orientalis. Eleven species from eight genera of biting flies were collected using unbaited Nzi traps. Tabanid species were present in all farms, with Dasybasis oculata (43.6 %) and D. circumdata (27.6 %) being the most abundant and widespread species. The effect of season on the mean count per trapping event was statistically significant and highest in the summer months for Lilaea fuliginosa and D. oculata, and the autumn months for D. circumdata, with no seasonal effect on the abundance of the undescribed Dasybasis spp. No biting flies were trapped during the winter months. Sucking (Linognathus vituli and Haematopinus eurysternus) and biting (Bovicola bovis) cattle lice were also collected from all farms with the latter detected in only one farm. PCR screening for T. orientalis of trapped hematophagous insects resulted in parasite detection in the tabanid and Stomoxyini flies, biting midges and sucking lice with the highest proportion of positive samples for Haematopinus eurysternus (4/4 pools) and H. irritans exigua (6/15 individuals). The detection of the parasite in these potential vectors indicates a possible role in the mechanical transmission of T. orientalis and may partly explain the ubiquitous presence of Theileria in areas where ticks are absent.

Spatial and temporal distribution of Culicoides species in the New England region of New South Wales, Australia between 1990 and 2018.

Culicoides are one of the smallest hematophagous flies measuring 1-5 mm in size with only females seeking blood for egg development. The present study investigated spatio-temporal distribution of Culicoides species trapped between 1990 and 2018 at 13 sites in the New England region of NSW, Australia using automated light traps. Trapping locations were divided into three subregions (tablelands, slopes and plains). Nineteen Culicoides species were identified. Culicoides marksi and C. austropalpalis were the most abundant and widespread species. Culicoides brevitarsis, the principal vector of livestock diseases in New South Wales comprised 2.9% of the total catch and was detected in 12 of the 13 locations in the study. Abundance as determined by Log10 Culicoides count per trapping event for the eight most abundant species did not vary significantly with season but trended towards higher counts in summer for C. marksi (P = 0.09) and C. austropalpalis (P = 0.05). Significant geographic variation in abundance was observed for C. marksi, C. austropalpalis and C. dycei with counts decreasing with increasing altitude from the plains to the slopes and tablelands. Culicoides victoriae exhibited the reverse trend in abundance (P = 0.08). Greater abundance during the warmer seasons and at lower altitudes for C. marksi and C. austropalpalis was indicative of temperature and rainfall dependence in this region with moderate summer dominance in rainfall. The Shannon-Wiener diversity index of species was higher on the tablelands (H = 1.59) than the slopes (H = 1.33) and plains (H = 1.08) with evenness indices of 0.62, 0.46 and 0.39 respectively. Culicoides species on the tablelands were more diverse than on the slopes and plains where C. marksi and C. austropalpalis dominated. The temporal and spatial variation in abundance, diversity and evenness of species reported in this diverse region of Australia provides additional insight into Culicoides as pests and disease vectors and may contribute to future modelling studies.

Endemic infection of cattle with multiple genotypes of Theileria orientalis on the Northern Tablelands of New South Wales despite limited presence of ticks.

Bovine theileriosis, caused by the Theileria orientalis complex, causes a mild persistent infection with the severity dependent on the infecting genotype and host exposure status. Clinical theileriosis was first detected on the Northern Tablelands of NSW in 2009 and a high prevalence of infection in cattle reported in 2013. However, the parasite was not genotyped and likely vectors not investigated. In response to ongoing clinical cases, here we identify the Theileria genotypes present in the region and potential vectors. Genotype-specific multiplex qPCR of 90 blood samples from eight farms revealed a 100 % prevalence of T. orientalis in individual cattle with concurrent infection with all three genotypes present in 73 % of cases. The prevalence of the pathogenic genotype (Ikeda) differed significantly between farms; however, the level of parasitemia was not affected by genotype or associated with clinical disease. Parasitaemia levels were higher in heifers than cows. Questing tick collection on six of the farms between November 2017 and May 2019 yielded 358 questing ticks from one farm, all of which were morphologically identified as Haemaphysalis bancrofti. Larvae accounted for 59 % of the ticks followed by nymphs (34 %) and adults (7%). Theileria was detected only in nymphs with Ikeda and Buffeli genotypes each being detected in one of four pools of ticks. The high prevalence of co-infection with three genotypes of T. orientalis indicates that they are now endemic in the region and confirms the lack of cross-protection between genotypes. This is the first detection of T. orientalis in questing H. bancrofti ticks: indicating that it may be a vector for T. orientalis in this region. However, the high prevalence of bovine infection is at odds with the absence of captured ticks or history of tick infestation on five of the six farms raising the possibility that other vectors or transmission pathways play key roles.