Bovine Theileriosis Caused by the Theileria orientalis Group

A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Parasitic Pathogens".

Deadline for manuscript submissions: closed (1 December 2022) | Viewed by 17166

Special Issue Editor


E-Mail Website
Guest Editor
NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, Woodbridge Rd, Menangle NSW 2568, Australia
Interests: Emerging veterinary diseases; veterinary disease epidemiology; genomics of microbes and parasites; molecular test development

Special Issue Information

Dear Colleagues,

Members of the of Theileria orientalis group are haemoparasites of cattle causing infections that can manifest either subclinically or as a severe disease characterised by anaemia, abortions and death. Bovine theileriosis caused by the T. orientalis group is an emerging disease across Asia, Australasia and, most recently, the United States and imposes a significant economic burden on cattle production in affected countries. The spectrum of clinical manifestations of the disease is a function of the parasite genotype, host immune status, environmental stressors and the presence of competent vectors.  

Like other Apicomplexan parasites, members of the Theileria orientalis group have a complex lifecycle and are transmitted by arthropods. The sexual phase of the organism’s lifecycle is supported by ticks of the genus Haemaphysalis, with a number of other arthropods implicated as mechanical transmitters. Transmission of disease in the absence of arthropod vectors is also possible, although severe disease is only reported in areas where vector ticks are observed. 

Recent outbreaks of bovine theileriosis have been associated with a distinct genotype of T. orientalis, Type 2 (Ikeda), and appear to have arisen from introductions of cattle into areas where Haemaphysalis ticks are already established. Recent genome studies suggest that T. orientalis Ikeda may represent an entirely separate species of Theileria, and there appears to be little cross-protection from this pathogenic genotype by some of the other more benign genotypes. 

Factors driving the host immune response to infection are currently unclear, although due to the intracellular nature of this parasite, immunity may be largely cell-mediated. Adult cattle in endemic areas appear to acquire long-lasting immunity; however, calves derive little passive immunity from dams and become highly parasitaemic between 1 and 2 months of age.  

There is currently no vaccine for bovine theileriosis caused by the T. orientalis group, and treatments are limited to chemotherapeutics that are only permitted for use in some countries due to prolonged retention of residues. 

This Special Issue is devoted to articles providing recent updates or reviews on bovine theileriosis caused by members of the T. orientalis group and aims to provide an update on the epidemiology, transmission, immunology, diagnosis and management of this disease.

Dr. Cheryl Jenkins
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Pathogens is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Theileria orientalis Ikeda
  • bovine theileriosis
  • epidemiology
  • genotype
  • ticks
  • transmission

Published Papers (9 papers)

Order results
Result details
Select all
Export citation of selected articles as:

Research

Jump to: Review

9 pages, 1328 KiB  
Article
Distribution and Prevalence of Theileria orientalis Genotypes in Adult Lactating Dairy Cows in South West Region of Western Australia
by Chi-Cheng Leong, Charlotte L. Oskam, Amanda D. Barbosa and Joshua W. Aleri
Pathogens 2023, 12(1), 125; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens12010125 - 12 Jan 2023
Cited by 1 | Viewed by 1363
Abstract
Bovine anaemia caused by Theileria orientalis group (BATOG) causes significant production and economic losses in Australia’s cattle industry. The pathogenic T. orientalis genotypes reported in Australian cattle are type 1 (Chitose) and type 2 (Ikeda). The present study aimed to determine the prevalence [...] Read more.
Bovine anaemia caused by Theileria orientalis group (BATOG) causes significant production and economic losses in Australia’s cattle industry. The pathogenic T. orientalis genotypes reported in Australian cattle are type 1 (Chitose) and type 2 (Ikeda). The present study aimed to determine the prevalence and distribution of T. orientalis genotypes in adult lactating cows in Western Australia (WA) dairy herds. A total of 100 whole blood samples from lactating cows from 10 farms were obtained and screened for T. orientalis using polymerase chain reaction (PCR). Sanger sequencing was subsequently used to characterise T. orientalis genotypes isolated from positive samples. A total of thirteen cows (13%; 95% CI: 7.1–21.2%) were positive for T. orientalis, and six out of ten farms (60%; 95% CI: 26.2–87.8%) housed at least one T. orientalis-positive cow. The distribution of T. orientalis was found to be wide and dense in the South west region of WA and the southern coast of WA. The predominant T. orientalis genotype identified was Ikeda (n = 11, 11%; 95% CI: 5.6–18.8%), while the Buffeli genotype was identified in WA for the first time, albeit at a low prevalence (n = 1, 1%; 95% CI: 0.0–5.4%). This study has provided useful epidemiological evidence on the prevalence and distribution of T. orientalis in adult lactating dairy cows in WA dairy farms, and on the importance of conducting widespread surveillance programs for the understanding of BATOG in WA. Full article
(This article belongs to the Special Issue Bovine Theileriosis Caused by the Theileria orientalis Group)
Show Figures

Figure 1

13 pages, 4645 KiB  
Article
Distribution of Theileria orientalis in Virginia Market Cattle, 2018–2020
by Alex Telionis, Kevin Lahmers, Michelle Todd, Amanda Carbonello, Charles C. Broaddus, Carolynn J. Bissett and Laura L. Hungerford
Pathogens 2022, 11(11), 1353; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11111353 - 15 Nov 2022
Cited by 4 | Viewed by 1441
Abstract
Theileria orientalis, genotype Ikeda, was recently detected in North America. Determining the emerging distribution of this pathogen is critical for understanding spread and developing management strategies. Whole blood samples were collected from cattle at Virginia livestock markets from September 2018 through December [...] Read more.
Theileria orientalis, genotype Ikeda, was recently detected in North America. Determining the emerging distribution of this pathogen is critical for understanding spread and developing management strategies. Whole blood samples were collected from cattle at Virginia livestock markets from September 2018 through December 2020. Animals were tested for T. orientalis using a universal and then genotype specific real-time PCR based on the MPSP gene. Prevalence for each genotype was analyzed for temporal trends and mapped by county. Spatial patterns were compared between genotypes and assessed for associations with habitat features, cattle movements through cattle markets and county proximity. Overall, 212 of 1980 samples tested positive for T. orientalis with an overall prevalence of 8.7% (172/1980) for genotype Ikeda, 1.8% (36/1980) for genotype Chitose, 0.2% (3/1980) for genotype Buffeli. The Ikeda genotype increased over time in northern and southwestern Virginia markets. The Ikeda and Chitose genotypes occurred in different regions, with little overlap, but for each genotype, spatial distribution was associated with a combination of cattle movements and environmental factors. Genotype specific qPCR testing and surveillance of cattle from across a wide area of Virginia are providing information on temporal, spatial, and other patterns for this emerging disease. Full article
(This article belongs to the Special Issue Bovine Theileriosis Caused by the Theileria orientalis Group)
Show Figures

Figure 1

8 pages, 961 KiB  
Article
Detection of Theileria orientalis Genotypes from Cattle in Kyrgyzstan
by Sezayi Ozubek, Mehmet Can Ulucesme, Veli Yılgor Cirak and Munir Aktas
Pathogens 2022, 11(10), 1185; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11101185 - 14 Oct 2022
Cited by 2 | Viewed by 1390
Abstract
The ikeda and chitose genotypes of Theileria orientalis, which for many years were thought to be benign, cause a disease that results in significant economic losses in the cattle industry. This study was carried out in order to determine the genotypes of [...] Read more.
The ikeda and chitose genotypes of Theileria orientalis, which for many years were thought to be benign, cause a disease that results in significant economic losses in the cattle industry. This study was carried out in order to determine the genotypes of T. orientalis in cattle in Kyrgyzstan, and 149 archived DNA samples known to be T. orientalis were analyzed by the PCR amplification of the major piroplasm surface protein (MPSP) gene region. Single-Strand Conformation Polymorphism (SSCP) analysis was performed to uncover the nucleotide changes in the archived DNA samples, and 15 samples showing different band profiles were subjected to sequence analysis. As a result of the sequence analysis, it was seen that the samples belonged to the buffeli and chitose A genotypes. In order to identify mixed genotypes, PCR was performed using primers specific for these genotypes, and buffeli (type 3), chitose (type 1) and buffeli+chitose were found to be positive in 26.2%, 2% and 71.8% of samples, respectively. As a result of this study, we showed the presence of buffeli (type 3) and chitose (type 1) genotypes of T. orientalis in cattle in Kyrgyzstan. Comprehensive epidemiological studies are needed to understand the clinical infections caused by the pathogenic chitose A and to determine the geographical distribution and different genotypes of T. orientalis. Full article
(This article belongs to the Special Issue Bovine Theileriosis Caused by the Theileria orientalis Group)
Show Figures

Figure 1

15 pages, 996 KiB  
Article
Characterisation of the Theileria orientalis Piroplasm Proteome across Three Common Genotypes
by Cheryl Jenkins, Melinda L. Micallef, Matthew P. Padula and Daniel R. Bogema
Pathogens 2022, 11(10), 1135; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11101135 - 30 Sep 2022
Cited by 1 | Viewed by 1681
Abstract
Theileria orientalis is an emerging apicomplexan pathogen of cattle occurring in areas populated by the principal vector tick, Haemaphysalis longicornis. Unlike transforming Theileria spp. that induce cancer-like proliferation of lymphocytes via their schizont stage, T. orientalis destroys host erythrocytes during its piroplasm [...] Read more.
Theileria orientalis is an emerging apicomplexan pathogen of cattle occurring in areas populated by the principal vector tick, Haemaphysalis longicornis. Unlike transforming Theileria spp. that induce cancer-like proliferation of lymphocytes via their schizont stage, T. orientalis destroys host erythrocytes during its piroplasm phase resulting in anaemia. The underlying pathogenic processes of T. orientalis infection are poorly understood; consequently, there are no vaccines for prevention of T. orientalis infection and chemotherapeutic options are limited. To identify antigens expressed during the piroplasm phase of T. orientalis, including those which may be useful targets for future therapeutic development, we examined the proteome across three common genotypes of the parasite (Ikeda, Chitose and Buffeli) using preparations of piroplasms purified from bovine blood. A combination of Triton X-114 extraction, one-dimensional electrophoresis and LC-MS/MS identified a total of 1113 proteins across all genotypes, with less than 3% of these representing host-derived proteins. Just over three quarters of T. orientalis proteins (78%) identified were from the aqueous phase of the TX-114 extraction representing cytosolic proteins, with the remaining 22% from the detergent phase, representing membrane-associated proteins. All enzymes involved in glycolysis were expressed, suggesting that this is the major metabolic pathway used during the T. orientalis piroplasm phase. Proteins involved in binding and breakdown of haemoglobin were also identified, suggesting that T. orientalis uses haemoglobin as a source of amino acids. A number of proteins involved in host cell interaction were also identified which may be suitable targets for the development of chemotherapeutics or vaccines. Full article
(This article belongs to the Special Issue Bovine Theileriosis Caused by the Theileria orientalis Group)
Show Figures

Figure 1

16 pages, 2866 KiB  
Article
Complete Genomes of Theileria orientalis Chitose and Buffeli Genotypes Reveal within Species Translocations and Differences in ABC Transporter Content
by Jerald Yam, Daniel R. Bogema, Melinda L. Micallef, Steven P. Djordjevic and Cheryl Jenkins
Pathogens 2022, 11(7), 801; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11070801 - 15 Jul 2022
Cited by 3 | Viewed by 1994
Abstract
Theileria orientalis causes losses to cattle producers in Eastern Asia, Oceania and, more recently, North America. One pathogenic genotype (Ikeda) has been sequenced to the chromosomal level, while only draft genomes exist for globally distributed Chitose and Buffeli genotypes. To provide an accurate [...] Read more.
Theileria orientalis causes losses to cattle producers in Eastern Asia, Oceania and, more recently, North America. One pathogenic genotype (Ikeda) has been sequenced to the chromosomal level, while only draft genomes exist for globally distributed Chitose and Buffeli genotypes. To provide an accurate comparative gene-level analysis and help further understand their pathogenicity, we sequenced isolates of the Chitose and Buffeli genotypes of T. orientalis using long-read sequencing technology. A combination of several long-read assembly methods and short reads produced chromosomal-level assemblies for both Fish Creek (Chitose) and Goon Nure (Buffeli) isolates, including the first complete and circular apicoplast genomes generated for T. orientalis. Comparison with the Shintoku (Ikeda) reference sequence showed both large and small translocations in T. orientalis Buffeli, between chromosomes 2 and 3 and chromosomes 1 and 4, respectively. Ortholog clustering showed expansion of ABC transporter genes in Chitose and Buffeli. However, differences in several genes of unknown function, including DUF529/FAINT-domain-containing proteins, were also identified and these genes were more prevalent in Ikeda and Chitose genotypes. Phylogenetics and similarity measures were consistent with previous short-read genomic analysis. The generation of chromosomal sequences for these highly prevalent T. orientalis genotypes will also support future studies of population genetics and mixed genotype infections. Full article
(This article belongs to the Special Issue Bovine Theileriosis Caused by the Theileria orientalis Group)
Show Figures

Figure 1

7 pages, 630 KiB  
Article
Effects of Theileria orientalis Infection on Health Status and Productivity of Dairy Cows Reared inside Barns
by Yuki Fukushima, Tomoya Minamino, Yoko Mikurino, Kazuyuki Honkawa, Yoichiro Horii, Takako Taniguchi, Hirohisa Mekata and Yosuke Sasaki
Pathogens 2021, 10(6), 650; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10060650 - 24 May 2021
Cited by 2 | Viewed by 1919
Abstract
The objective of the present study was to investigate the effects of Theileria orientalis on the severity of anemia, the prevalence of disease within 21 days after calving and productivity in cows raised inside barns. This longitudinal observational study, which was conducted on [...] Read more.
The objective of the present study was to investigate the effects of Theileria orientalis on the severity of anemia, the prevalence of disease within 21 days after calving and productivity in cows raised inside barns. This longitudinal observational study, which was conducted on a commercial dairy farm in Japan, involved 627 Holstein cows subjected to PCR analysis for T. orientalis. In study 1, we collected blood samples from 156 sick cows within 21 days after calving, and we found the prevalence of T. orientalis infection to be 65.4%. In study 2, we randomly selected 471 cows during the dry period and collected blood samples to conduct PCR analysis for T. orientalis and determined the prevalence of T. orientalis infection to be 69.0%. Compared with the values for the T. orientalis-uninfected group, the T. orientalis-infected cows had significantly decreased hemoglobin concentrations and hematocrit, but there were no differences in the other complete blood count indexes between the two groups. In addition, there were no differences in productivity and the prevalence of major diseases between the T. orientalis-infected and uninfected cows. In summary, T. orientalis had few effects on anemia, productivity and the health of cows raised inside a barn. Full article
(This article belongs to the Special Issue Bovine Theileriosis Caused by the Theileria orientalis Group)
Show Figures

Figure 1

Review

Jump to: Research

14 pages, 995 KiB  
Review
Epidemiology and Transmission of Theileria orientalis in Australasia
by Biniam T. Lakew, Steve Eastwood and Stephen W. Walkden-Brown
Pathogens 2023, 12(10), 1187; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens12101187 - 22 Sep 2023
Cited by 2 | Viewed by 1143
Abstract
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue Bovine Theileriosis Caused by the Theileria orientalis Group)
Show Figures

Figure 1

15 pages, 5415 KiB  
Review
Review of the New Zealand Theileria orientalis Ikeda Type Epidemic and Epidemiological Research since 2012
by Kevin Lawrence, Kristene Gedye, Andrew McFadden, David Pulford, Allen Heath and William Pomroy
Pathogens 2021, 10(10), 1346; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10101346 - 19 Oct 2021
Cited by 8 | Viewed by 2104
Abstract
This article sets out to document and summarise the New Zealand epidemic and the epidemiological research conducted on the epizootic of bovine anaemia associated with Theileria orientalis Ikeda type infection, which began in New Zealand in August 2012. As New Zealand has no [...] Read more.
This article sets out to document and summarise the New Zealand epidemic and the epidemiological research conducted on the epizootic of bovine anaemia associated with Theileria orientalis Ikeda type infection, which began in New Zealand in August 2012. As New Zealand has no other pathogenic tick-borne cattle haemoparasites, the effects of the T. orientalis Ikeda type infection observed in affected herds and individual animals were not confounded by other concurrent haemoparasite infections, as was possibly the case in other countries. This has resulted in an unbiased perspective of a new disease. In addition, as both New Zealand’s beef and dairy cattle systems are seasonally based, this has led to a different epidemiological presentation than that reported by almost all other affected countries. Having verified the establishment of a new disease and identified the associated pathogen, the remaining key requirements of an epidemiological investigation, for a disease affecting production animals, are to describe how the disease spreads, describe the likely impacts of that disease at the individual and herd level and explore methods of disease control or mitigation. Full article
(This article belongs to the Special Issue Bovine Theileriosis Caused by the Theileria orientalis Group)
Show Figures

Figure 1

14 pages, 344 KiB  
Review
Approaches to Integrated Parasite Management (IPM) for Theileria orientalis with an Emphasis on Immunity
by David Lyall Emery
Pathogens 2021, 10(9), 1153; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10091153 - 07 Sep 2021
Cited by 8 | Viewed by 2845
Abstract
Integrated parasite management (IPM) for pests, pathogens and parasites involves reducing or breaking transmission to reduce the impact of infection or infestation. For Theileria orientalis, the critical impact of infection is the first wave of parasitaemia from the virulent genotypes, Ikeda and [...] Read more.
Integrated parasite management (IPM) for pests, pathogens and parasites involves reducing or breaking transmission to reduce the impact of infection or infestation. For Theileria orientalis, the critical impact of infection is the first wave of parasitaemia from the virulent genotypes, Ikeda and Chitose, associated with the sequelae from the development of anaemia. Therefore, current control measures for T. orientalis advocate excluding the movement of naïve stock from non-endemic regions into infected areas and controlling the tick Haemaphysalislongicornis, the final host. In Australia, treatment of established infection is limited to supportive therapy. To update and expand these options, this review examines progress towards prevention and therapy for T. orientalis, which are key elements for inclusion in IPM measures to control this parasite. Full article
(This article belongs to the Special Issue Bovine Theileriosis Caused by the Theileria orientalis Group)
Back to TopTop