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Theileria orientalis: A review a
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J. G. Watts , M. C. Playford & K. L. Hickey a
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Ministry for Primary Industries, PO Box 2526, Wellington, New Zealand
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Dawbuts Pty Ltd, PO Box 1118, Camden, NSW 2570, Australia Accepted author version posted online: 06 Jul 2015.
Click for updates To cite this article: J. G. Watts, M. C. Playford & K. L. Hickey (2015): Theileria orientalis: A review, New Zealand Veterinary Journal, DOI: 10.1080/00480169.2015.1064792 To link to this article: http://dx.doi.org/10.1080/00480169.2015.1064792
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Publisher: Taylor & Francis & New Zealand Veterinary Association Journal: New Zealand Veterinary Journal DOI: 10.1080/00480169.2015.1064792
Review Article
Theileria orientalis: A review Watts JGa*, Playford MCb and Hickey KLa a
Ministry for Primary Industries, PO Box 2526, Wellington, New Zealand Dawbuts Pty Ltd, PO Box 1118, Camden NSW 2570, Australia * Author for correspondence. Email: [email protected]
Theileria orientalis (also known historically as T. sergenti and T. buffeli) is responsible for benign
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or non-transforming theileriosis, and exerts its major effect through erythrocyte destruction. The life cycle of T. orientalis is essentially similar to that of other Theileria species, except that the schizonts do not induce transformation and fatal lymphoproliferation. The pathogenesis of anaemia as a result of infection is not clearly established and may be multifaceted. Clinical signs of weakness, reluctance to walk and abortion are early but non-specific indications of disease,
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particularly if accompanied by a history of cattle being moved. Physical examination may reveal
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pallor (pale eyes, vaginal mucosa), pyrexia, and elevated heart and respiratory rates. T. orientalis is an economically important parasite of cattle in New Zealand, Australia and Japan, especially where naïve animals are introduced into an endemic area or in animals under stress. Increased awareness
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of the risks posed by the parasite is required to enable management practices to be implemented to minimise its impact.
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Abstract
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KEY WORDS: Theileria orientalis, anaemia, cattle, theileriosis, tick-borne protozoal disease
MPSP Major piroplasm surface protein
Introduction The objective of this paper is to provide a review of the tick-borne protozoan parasite Theileria orientalis, and to describe the experiences of three countries that have been significantly affected by 1
it, New Zealand, Australia and Japan, including how the parasite behaves in each country and the management that has been applied. Theileria orientalis has a worldwide distribution and is only known to cause disease in cattle. Other Theileria species are known to cause disease in other species including horses, sheep, buffalo and yak. Most theileriae are confined to Asia or Africa, corresponding to the geographical distribution of their vector ticks, except for the worldwide distribution of the T. sergenti/T. buffeli/T. orientalis complex.
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Six species of Theileria are recognised to infect Bovidae. T. parva and T. annulata are known as
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transforming Theileria spp. due to their ability to transform the host lymphoid cells (von Schubert et al. 2010) and are the two most pathogenic and consequently economically important species
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worldwide. The other species cause benign or non-transforming theileriosis. These exert their major orientalis, the focus of this review.
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Taxonomy of Theileria orientalis
Theileria orientalis is part of the T. sergenti/T. buffeli/T. orientalis group of non-transforming Theileria parasites. The taxonomic status of this group has been debated for many years (Sugimoto and Fujisaki 2002).These organisms were previously designated according to geographical origin
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(Jeong et al. 2010), with T. sergenti in Japan, T. buffeli in Australia and T. orientalis in Europe and
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elsewhere (Kawazu et al. 1992). Some studies suggested that T. sergenti should be separated from T. buffeli and T. orientalis on the basis of their serological dissimilarities and differences in transmissibility (Fujisaki 1992; Kawazu et al. 1992).
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Theileria sergenti is an invalid name taxonomically as it has been used to previously describe a parasite of sheep (Morel and Uilenberg 1981). In 1985 it was suggested that this group of Theileria parasites are the same species, based on serological and morphological identities, and it was
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pathological effects through erythrocyte destruction (Eamens et al. 2013c), and include T.
proposed T. orientalis be used to name the group (Uilenberg 1985).
Molecular studies, in the form of major piroplasm surface protein (MPSP) gene sequencing, have been used as a practical means of classification, as the strain types correlate with virulence. Based on molecular studies, MPSP and 18S rDNA sequences, the T. sergenti/T. buffeli/ T. orientalis group
of Theileria parasites can be designated as one group (Kamau et al. 2011; Sivakumar et al. 2014), hereafter known simply as T. orientalis. Within this species four major MPSP types were initially identified; p32 (Type 5), Buffeli, Chitose and Ikeda, with the latter being strongly associated with clinical disease in Australia, Japan and 2
New Zealand (Eamens et al. 2013c). Further phylogenetic analysis of the T. orientalis MPSP gene sequences revealed 11 allelic types (Sivakumar et al. 2014).
Life cycle and pathogenesis The genus Theileria comprises tick-transmitted protozoa characterised by schizonts in lymphoid cells and piroplasms in red blood cells of the vertebrate host. Transmission of T. orientalis occurs through the feeding of infected ticks of the Haemaphysalis genus (Riek 1982; Stewart 1987). New Zealand has only one livestock-infesting tick present, H. longicornis (Heath 2015), and this is
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considered to be the vector of T. orientalis in this country (McFadden et al. 2011). Ticks are infected while feeding on an infected host whose erythrocytes contain Theileria spp. piroplasms. The ingested erythrocytes are lysed in the gut lumen. A proportion of the released
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spherical zygote results, which invades a gut epithelial cell. The parasite then undergoes meiotic division and differentiates into a motile kinete. During or just after the tick moults to the next instar
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the kinete escapes from the gut cell and gains access to the haemocoel. It then migrates to the salivary glands and invades a specific population of salivary gland cells. It is in the salivary glands where the only multiplication stage of the parasite in the tick occurs (sporogony) and the parasite develops into a multinucleate sporont (Shaw 2002). Sporozoite development occurs during tick
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mammalian host (Shaw 2002).
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feeding and results in many thousands of sporozoites, which are released slowly into the
Transstadial transmission but not transovarial transmission occurs in ticks (Stewart et al. 1996). There is also a possibility that transmission could occur due to biting flies (Stomoxys calcitrans) and
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sucking lice (Linognathus vituli), or via vaccination needles(Fujisaki et al. 1993), but the life cycle is not maintained in lice or flies. The infected ticks transmit the infective sporozoite stage in their saliva as they feed. The
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piroplasms differentiate into gametocytes and fertilisation (syngamy) occurs in the gut lumen. A
sporozoites then invade leucocytes and within a few days develop into schizonts. In a study on H.
longicornis recovered from a paddock where infected cattle were grazing in Japan, about 20% were
found to have T. orientalis in their salivary glands (Kamio et al. 1990). At approximately 10 days post inoculation with sporozoites, schizonts can be detected transiently in the lymph nodes, spleen and liver. Schizont-infected cells are not usually found in the peripheral blood and the schizont does not appear to play a major role in pathogenesis (Sugimoto and Fujisaki 2002).
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The lymphoid life stage of T. orientalis (Buffeli) has been demonstrated by Stewart et al. (1988). After experimental infection of cattle, macroschizonts were demonstrated in Giemsa-stained lymph node preparations for between 6 and 20 days following tick infestation. The presence of schizonts was confirmed by immunofluorescence with sera from known infected animals. Microschizonts were seen infrequently. Piroplasms can be detected in the erythrocytes at approximately 10 days post inoculation. At this time transient pyrexia may also be observed in addition to the development of anaemia. In immunologically exposed animals there is generally a low level of parasitaemia (Shimizu et al.
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1992). Animals do recover from the infection although the parasites may persist, possibly for life. Consequently, relapses can occur during times of stress such as pregnancy, lactation or rapid
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changes in environmental conditions (Sugimoto and Fujisaki 2002).
erythrocytes (Kawamoto et al. 1990), but the pathogenesis of anaemia consequent to infection is not
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clearly established and may be multifaceted (Stockham et al. 2000). Studies of erythrocyte survival in infected calves demonstrated that both infected and uninfected erythrocytes have reduced survival (Yagi et al. 1991). An immune-mediated process for erythrocyte destruction has been suggested. However, other studies indicate that erythrocyte destruction can occur without immunoglobulin or complement involvement (Hagiwara et al. 1995). Shiono et al. (2001)
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demonstrated that the progress of anaemia is associated with elevated levels of methaemoglobin, a
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product of haemoglobin oxidation. An increase in methaemoglobin causes the release of superoxide radicals from haemoglobin which could possibly result in oxidative damage of erythrocytes and
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their removal from the circulation by the reticuloendothelial system (Sugimoto and Fujisaki 2002).
Clinical signs
Clinical signs of weakness, reluctance to walk and abortion are early but non-specific indications of
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Theileria orientalis exerts its major effect due to its piroplasmic form causing destruction of
infection with T. orientalis, particularly if accompanied by a history of cattle being moved. Physical
examination may reveal pallor (pale eyes, vaginal mucosa), pyrexia, and elevated heart and respiratory rates (Izzo et al. 2010). Blood samples in EDTA can be collected for laboratory analysis.
Thin smears under Giemsa stain show T. orientalis parasites in variable numbers of erythrocytes (0.5–30%). Packed cell volume can range from near normal down to 8% in severely-affected cases (Irwin 2013). The Buffeli type doesn’t appear to be associated with anaemia, however the Chitose and Ikeda types are associated with anaemia (Eamens et al. 2013c). In surveys of cattle in New South Wales, Queensland and Victorian, Chitose and Buffeli appear most commonly in non-clinical isolates, but may appear alongside Ikeda in clinically-affected animals (Eamens et al. 2013a). 4
Cattle are thought to become infected within three weeks of being placed on pasture harbouring infected vectors and begin to develop anaemia and related clinical signs soon after (Nakamura et al. 2010). Disease is more frequently seen when naive animals are introduced into an endemic area or when infected animals are introduced to a herd where a competent vector is present but Theileria species are not present or only at a low prevalence (Eamens et al. 2013a) It has been suggested that combined infections with different strains of T. orientalis may assist the parasite to sustain infection in the cattle host by presenting a variety of immune targets rather than a
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few (Eamens et al. 2013c).
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Diagnosis
Theileriosis can be diagnosed by light microscopic examination of dried Giemsa-stained blood
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be very low, in the order of 0.02–0.03% (Kamio et al. 1990; Shimizu et al. 1992). Small piroplasms of various shapes can be observed in the erythrocytes (Stockham et al. 2000). Erythrocyte infection al. 2010; McFadden et al. 2011).
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>1% and up to 30% are generally associated with severe anaemia and related clinical signs (Izzo et
Serological methods including ELISA to detect Theileria spp. antibodies in the blood of hosts was widely used in Japan for both diagnostic (Ota et al. 2009) and epidemiologic purposes (Minami et
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al. 1980). In one study, ELISA was found to be more sensitive than light microscopy for established
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infections, but the reverse was true for new infections, as seronegative/microscopy-positive cows checked 2 months later had seroconverted (Shimizu et al. 1992). Serology (indirect fluorescent antibody test) has also been used for survey work in Australia (Stewart et al. 1992).
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Specific diagnosis of theileriosis now relies on PCR assays to identify the MPSP (Kim et al. 1998). This method can detect infection in cattle 2 weeks before infected erythrocytes are visible by light microscopy (Ota et al. 2009) and also allows differentiation of different MPSP types that may be
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smears (Biddle et al. 2013). In infected but non-clinically-affected cattle erythrocyte invasion may
associated with pathogenicity or geographic specificity (Kubota et al. 1996; Kim et al. 2004). Refinement of PCR methods has resulted in highly sensitive and specific tests including the
multiplexed tandem PCR (Perera et al. 2015).
Bovine theileriosis in New Zealand The first published report of T. orientalis in New Zealand was in 1984 (James et al. 1984), and explained that the occurrence of this parasite in New Zealand was unsurprising, as at that time cattle were imported from Britain and Australia where the parasite was known to occur. Despite the parasite not being identified in New Zealand prior to this time it was likely to already have been 5
present for several years. The reason it remained undetected until that point is open to conjecture (James et al. 1984). Following the first description of T. orientalis in New Zealand, the number of reported cases increased until 1985 when the Whangarei Animal Health Laboratory diagnosed 60 cases or outbreaks, with the most common presenting signs being ill thrift, drop in milk and meat production, anorexia, malaise, depression, and diarrhoea. This disease then disappeared before reemerging 4 years later in Wairoa and Northland. It was suggested that T. orientalis was widespread in New Zealand and when environmental conditions are appropriate for the multiplication of ticks,
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and when susceptible animals are present, the disease appears (Thompson 1991).
Rawdon et al. (2006) described the investigation of jaundice, pyrexia, collapse, and death in a 20-
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month-old steer from north Waikato. Examination of blood smears from this individual revealed other causes of haemolytic anaemia and concluded that T. orientalis was the responsible agent and
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the primary cause of death.
In 2009 one outbreak of anaemia associated with infection by Type 1 (Chitose) strain of T. orientalis in a group of cattle moved from South Otago to Northland was described as affecting 38% of investigated animals with 1% mortality (McFadden et al. 2011). This investigation concluded that members of the T. orientalis group present in New Zealand were capable of causing
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disease in cattle not necessarily debilitated by another disease. In December 2012, the Ministry for Primary Industries’ Animal Health Laboratory first identified T. orientalis Ikeda, which had not previously been identified in New Zealand. Since late 2012
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outbreaks of anaemia associated with T. orientalis Ikeda have been reported in dairy and beef cattle herds located in multiple regions (Northland, Auckland, Waikato, Taranaki, Manawatu/Wanganui, Bay of Plenty and Wellington). Outside the known endemic tick areas the impact of the disease
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over 50% of erythrocytes to be parasitised with T. orientalis. The authors of this study ruled out
appears to be much less severe. The number of outbreaks in cattle herds has steadily increased since T. orientalis Ikeda was first identified in New Zealand (McFadden et al. 2013). In the early stages of the epidemic, genotyping of T. orientalis from these outbreaks was carried out and one was identified as T. orientalis Ikeda strain. Other strains present were T. orientalis Chitose and T. orientalis Buffeli. The Ikeda strain reportedly has greater pathogenicity than other endemic strains present in New Zealand (Chitose and buffeli) (McFadden et al. 2013).
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It is not possible to say how long the Ikeda strain has been present in New Zealand. Testing of stored serum samples for T. orientalis organisms, prior to December 2012, from investigations from Northland collected since 2008 failed to detect the Ikeda strain (McFadden et al. 2013).
Bovine theileriosis in Australia Infection of cattle in Australia with T. orientalis was first recorded in 1910 (Seddon and Albiston 1966). Distribution is widespread, with herd and individual animal seroprevalence in Queensland of 75% and 41% respectively (Stewart et al. 1992). Infection has also been detected in cattle across
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solitary location in southwest Western Australia (Anonymous 2014).
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New South Wales (Eamens et al. 2013b), eastern and northern Victoria (Perera et al. 2013) and in a
Until the mid-2000s infection was considered benign (Mahoney 1994) with only occasional reports
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Wales with increasing frequency from 2006–2010 (Izzo et al. 2010) with the number of clinical cases climbing until 2013 (Eamens et al. 2013b). In 2008 there were 52 reported cases of clinical
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theileriosis in New South Wales alone, accounting for an estimated 800 deaths (Paul Freeman,1 pers. comm.). In a population of 460 cattle on 46 randomly-selected beef farms in the New England district of New South Wales, 110 (22% ) cattle and 33 (72%) properties were found to be positive on light microscopy (Biddle et al. 2013). In Victoria, occasional cases had been observed
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historically, but the first confirmed case with the Ikeda strain was seen in 2011 (Islam et al. 2011),
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with dozens of cases since reported.
Fundamental research was conducted on theileriosis by the Wacol Tick Fever Centre in the 1980s, due to incidental infection with what was then known as T. buffeli causing contamination of the live
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tick fever (Babesia/Anaplasma) vaccine. As a result, effective means were devised for treating infected calves prior to them becoming vaccine donors, along with the clarification of the parasite’s epidemiological features (Stewart et al. 1988, 1990a).
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of clinical disease (Rogers and Callow 1966). Clinical theileriosis was reported in New South
Genotypes of T. orientalis in Australia
Theileria orientalis found in Australia was, until recently, described as T. buffeli (Gubbels et al. 2000). The species is now accepted to be T. orientalis, the same as that found in East Asia. Buffeli is now used as a descriptor of the strain found mainly in benign cases, rather than as a species name. Historically, typing showed serological differences (detected by ELISA) between Australian isolates and those from Japan and Britain (Kawazu et al. 1992). Queensland (Warwick) isolates of T. orientalis were identified as T. buffeli and further evidence for them to be considered separate 1P
Freeman, NSW DPI, Wollongbar, Australia
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biologically was provided by the fact that transmission was possible in Australian marsupial ticks found in Queensland and northern New South Wales, but not H. longicornis (Stewart et al. 1996). Analysis of MPSP by PCR in 1995 revealed that Australian isolates showed proteins characteristic for Buffeli and Chitose, but not the Ikeda type often associated with virulence in Japan and other Asian countries (Kubota et al. 1996). In 2011 the first evidence was provided that the Ikeda strain was present and associated with virulent disease in New South Wales cattle (Kamau et al. 2011). This was confirmed separately in New South Wales (Eamens et al. 2013a) and Victoria (Islam et al. 2011). While Buffeli is the dominant strain found in Queensland, in Victoria it was only isolated
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from 2.4% of 213 cattle tested. In contrast, Ikeda was isolated from 91.1% of these cattle (Perera et al. 2013). Mixed infection with two or more strains is common and there may be antigenic drift
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within an isolate.
Until the 1980s T. orientalis in Australia was thought to be spread by the cattle tick Rhipicephalus
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(Boophilus) australis (formerly B. microplus). However transmission studies using H. longicornis and H. bancrofti showed that these two species were capable of transmitting T. orientalis, while B. microplus, Ixodes holocyclus and Amblyomma triguttatum were not (Riek 1982). However, in Queensland the T. buffeli life cycle was shown to involve either of two species of
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native tick, H. bancrofti and H. humerosa, but not H. longicornis (Stewart 1987). In southern New South Wales and Victoria, where H. bancrofti and H. humerosa are rare or non-existent, the vector
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is assumed to be H. longicornis. Strain differences were shown experimentally to affect vector transmissibility, in that Australian H. longicornis could only transmit T. sergenti and could not
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transmit Australian T. buffeli, while Japanese H. longicornis could transmit both (Fujisaki 1992). Further transmission studies need to be conducted on recent isolates of T. orientalis from Australia, including Chitose and Ikeda strains, to confirm transmissibility differences.
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Vectors of T. orientalis in Australia
The Australian strain of H. longicornis is assumed to originate from northern Japan, due to its parthenogenetic nature (Hoogstraal et al. 1968; Herrin and Oliver 1974). This species is distributed
widely across temperate Eastern Australia, as far south as East Gippsland and the Murray Valley in Victoria and north to Gayndah in Queensland. It has also been isolated from inland sites such as Tenterfield and Young, New South Wales (Roberts 1962), and in Western Australia. Although primarily considered a cattle tick, it commonly infests many other species. In Australia it has been isolated from horses, sheep, cats, dogs and pigs, as well as native animals such as the wallaroo (Macropus robustus) and bandicoot (Isoodon macrourus) (Roberts 1962). 8
Other vectors of theileriosis such as March flies (Tabanidae), mosquitoes or sucking lice have been suggested, as disease outbreaks have occurred without ticks being observed (Islam et al. 2011; Bailey 2013b; Irwin 2013). However, due to their three-host life cycle, Haemaphysalis spp. may infest cattle in low numbers without being obvious to the herd manager (Perera et al. 2013). In Japan, H. longicornis is considered to be the main biological vector of T. orientalis, but it is also transmitted mechanically by sucking lice (Fujisaki et al. 1993) and blood-feeding midges (Ceratopogonidae) (Onoe et al. 1994). This raises the possibility of mechanical transmission in Australia, either by arthropod vectors or via fomites such as vaccination needles, eartag pliers or
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rectal examination gloves. Nevertheless, studies have show that observation of ticks is correlated with detection of T. orientalis. (Burney and Lugton 2010), and treatment of cattle for ticks was associated with a lower detection of T. orientalis compared to farms that did not treat (Biddle et al.
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Epidemiology of T. orientalis in Australia
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Cattle movement is a prominent feature of the cases of T. orientalis infection reported in 2006– 2012. Many of the outbreaks of clinical disease in 2006–2010 were associated with cattle that had been moved to the coast from drier inland areas (Izzo et al. 2010). Foci of cases were initially seen in coastal New South Wales, (Burney and Lugton 2010) but reports of cases in inland areas after introduction of coastal cattle were typical of the second phase of the outbreak (Bailey 2011). Cases
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occurred in inland areas where none had previously been recorded and ticks were either not noted or
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considered rare. For example, cows on the point of calving in a herd of 122 cattle brought from Tasmania (and therefore presumed to be naïve) began to shown signs of theileriosis including 10
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deaths on arrival on farm at Moree, in inland northwest New South Wales (Irwin 2013). More recently, severe morbidity and high mortality has been noted in calves 6–14 weeks of age, especially on properties where theileriosis has previously been diagnosed in adult cattle (Ball 2013; Eastwood 2013). The economic cost of theileriosis outbreaks in Australia has been assessed by
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2013).
Perera et al. (2013, 2014).
Treatment and control
Attempts have been made to treat bovine theileriosis with imidocarb, oxytetracyclines and halofuginone, with equivocal results. Under research conditions, combinations of primaquine and buparvaquone, or primaquine with halofuginone totally eliminated infection of T. buffeli from splenectomised calves (Stewart et al. 1990b). In other countries buparvaquone alone has been used with success (Ozawa et al. 1988). However these products are either unavailable in Australia 9
(primaquine and buparvaquone) or in a formulation unsuitable for economical treatment of adult cattle (halofuginone). Trials on artificially-infected splenectomised calves showed that buparvaquone at a dose rate of 2.5 mg/kg injected once I/M was an adequate treatment for Buffeli, Chitose and Ikeda variants of T. orientalis (Carter 2011). However, tissue depletion studies for buparvaquone in cattle, conducted so that it could be used under permit in clinically-affected cattle in Australia, found that residues were present as long as 147 days after administration (Bailey 2013a). This is the main reason why
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buparvaquone is not used to treat cases in Australia.
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A noted above, tick control has been linked with a lower detection of T. orientalis. The only
products registered in Australia for control of H. longicornis are short-acting dips and sprays
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containing deltamethrin and ethion in combination, amitraz, chlorphenvinphos and cypermethrin in to 10 days. Flumethrin pour-on formulation is not available to treat cattle in Australia (Ottaway and
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Cook 2005). Because of this many veterinarians are recommending the off-label use of pour-on or injectable macrocyclic lactone products in the hope of providing longer protection for cattle on introduction to suspected danger areas.
Bovine theileriosis in Japan
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Theileriosis is recognised wherever cattle are found across the entire Japanese archipelago. The
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dominant species is currently referred to as T. orientalis, with most references prior to 2005 naming it as T. sergenti (Fujisaki 1992). It is now accepted that these names, as well as T. buffeli, all describe the same species (Uilenberg 2011) which can be characterised using molecular techniques
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targeting the MPSP antigens.
Vectors of T. orientalis in Japan
The main vector, H. longicornis (Itagaki and Ohishi 1990), is commonly isolated from cattle but
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combination, as well as flumethrin spray (aqueous solution) which has a period of protection of up
also infests dogs and other mammalian and bird species (Shimada et al. 2003). A characteristic of H. longicornis in Japan is that north of Tokyo mostly females are found and reproduction is thought to be through parthenogenesis, while in warmer southern areas males and females are found and reproduction is sexual (Itagaki and Ohishi 1990). In the southern islands of Okinawa the vector is H. mageshimaensis (Zakimi et al. 2006). Infection is also thought to be transferred mechanically, either by vectors such as tabanids or sucking lice, or alternatively by transplacental infection of calves (Onoe et al. 1994). New strains of T. orientalis are thought to have been introduced into Japan from Australia with imported cattle in the 1990s (Kawazu et al. 1995). A recent study using 10
PCR to isolate T. orientalis DNA from ticks collected in Okinawa and Hokkaido has shown that other H. megaspinosa and H. douglasi, as well as two species of Ixodes, are potential vectors (Yokoyama et al. 2012) Epidemiology of theileriosis in Japan
Clinical disease is reported as being seen mainly in dairy cattle in summer and autumn, usually associated with grazing on pasture, with a possible role of wildlife hosts contaminating pastures with infected ticks (Nishino et al. 2008). However, disease is also seen in confined cattle (Shimizu et al. 1992). Beef cattle, particularly the indigenous Wagyu breed, are considered less susceptible to
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infection (Higuchi et al. 1997). Groups of grazing Holstein heifers were monitored in a national study of 85 herds across 30 of Japan’s 50 prefectures. The incidence of infection and number of
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heifers requiring treatment were highest in southern regions (41.1% and 38.6%) and lowest in 2001).
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Treatment
As stress due to pregnancy, exercise or concurrent nutritional challenge was found to be a contributor to the expression of clinical theileriosis, supportive therapy including I/V fluids, nutritional supplements, and blood transfusion may be used. Iron dextran solution injected I/M over
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3 days was also found to aid recovery from infection (Nakamura et al. 2010).
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Primaquine phosphate and pamaquine were widely used against T. orientalis in the 1970s and 1980s. However, the efficacy of these two compounds under field conditions in Japan declined (Minami et al. 1985) leading to clinicians stopping their use. Buparvaquone has been successfully
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trialled on clinical cases in Japan but not registered (Ozawa et al. 1988). Tetrocarcin was also found to be effective in reducing parasitaemia but not registered (Ohtomo et al. 1985), while imidocarb was not found to be useful in treating infections (Minami et al. 1985).
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northern regions (18% and 6.2%), in proportion to observed tick numbers on cattle (Yamane et al.
Use of a live vaccine based on piroplasms was terminated due to the accidental transmission of potential pathogens including bovine leukaemia virus (Onuma et al. 1998). This led to attempts to create a subunit vaccine (Onuma et al. 1997). This has remained elusive to date, but studies on the T. orientalis genome to find a target site are continuing (Hayashida et al. 2012). As a preventive measure, attention has turned to tick control. Cattle are routinely treated with long-acting preparations of synthetic pyrethroids prior to putting out to graze on pasture, a strategy that has proved effective in reducing tick numbers and incidence of infection (Shimizu et al. 2000).
Conclusion 11
Theileria orientalis is an economically important parasite of cattle in New Zealand, Australia and Japan, especially where naïve animals are introduced into an endemic area or in animals under stress. Awareness of the risks posed by the parasite is required to enable management practices to be implemented to minimise its impact. Management of the tick vector may reduce the incidence of the disease, as will reducing stress on stock.
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* Non-peer-reviewed
Submitted 01 September 2014
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Accepted for publication 27 May 2015
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First published online [insert date]
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New Zealand Veterinary Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tnzv20
Theileria orientalis: A review a
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J. G. Watts , M. C. Playford & K. L. Hickey a
a
Ministry for Primary Industries, PO Box 2526, Wellington, New Zealand
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Dawbuts Pty Ltd, PO Box 1118, Camden, NSW 2570, Australia Accepted author version posted online: 06 Jul 2015.
Click for updates To cite this article: J. G. Watts, M. C. Playford & K. L. Hickey (2015): Theileria orientalis: A review, New Zealand Veterinary Journal, DOI: 10.1080/00480169.2015.1064792 To link to this article: http://dx.doi.org/10.1080/00480169.2015.1064792
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Review Article
Theileria orientalis: A review Watts JGa*, Playford MCb and Hickey KLa a
Ministry for Primary Industries, PO Box 2526, Wellington, New Zealand Dawbuts Pty Ltd, PO Box 1118, Camden NSW 2570, Australia * Author for correspondence. Email: [email protected]
Theileria orientalis (also known historically as T. sergenti and T. buffeli) is responsible for benign
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or non-transforming theileriosis, and exerts its major effect through erythrocyte destruction. The life cycle of T. orientalis is essentially similar to that of other Theileria species, except that the schizonts do not induce transformation and fatal lymphoproliferation. The pathogenesis of anaemia as a result of infection is not clearly established and may be multifaceted. Clinical signs of weakness, reluctance to walk and abortion are early but non-specific indications of disease,
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particularly if accompanied by a history of cattle being moved. Physical examination may reveal
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pallor (pale eyes, vaginal mucosa), pyrexia, and elevated heart and respiratory rates. T. orientalis is an economically important parasite of cattle in New Zealand, Australia and Japan, especially where naïve animals are introduced into an endemic area or in animals under stress. Increased awareness
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of the risks posed by the parasite is required to enable management practices to be implemented to minimise its impact.
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Abstract
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KEY WORDS: Theileria orientalis, anaemia, cattle, theileriosis, tick-borne protozoal disease
MPSP Major piroplasm surface protein
Introduction The objective of this paper is to provide a review of the tick-borne protozoan parasite Theileria orientalis, and to describe the experiences of three countries that have been significantly affected by 1
it, New Zealand, Australia and Japan, including how the parasite behaves in each country and the management that has been applied. Theileria orientalis has a worldwide distribution and is only known to cause disease in cattle. Other Theileria species are known to cause disease in other species including horses, sheep, buffalo and yak. Most theileriae are confined to Asia or Africa, corresponding to the geographical distribution of their vector ticks, except for the worldwide distribution of the T. sergenti/T. buffeli/T. orientalis complex.
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Six species of Theileria are recognised to infect Bovidae. T. parva and T. annulata are known as
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transforming Theileria spp. due to their ability to transform the host lymphoid cells (von Schubert et al. 2010) and are the two most pathogenic and consequently economically important species
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worldwide. The other species cause benign or non-transforming theileriosis. These exert their major orientalis, the focus of this review.
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Taxonomy of Theileria orientalis
Theileria orientalis is part of the T. sergenti/T. buffeli/T. orientalis group of non-transforming Theileria parasites. The taxonomic status of this group has been debated for many years (Sugimoto and Fujisaki 2002).These organisms were previously designated according to geographical origin
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(Jeong et al. 2010), with T. sergenti in Japan, T. buffeli in Australia and T. orientalis in Europe and
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elsewhere (Kawazu et al. 1992). Some studies suggested that T. sergenti should be separated from T. buffeli and T. orientalis on the basis of their serological dissimilarities and differences in transmissibility (Fujisaki 1992; Kawazu et al. 1992).
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Theileria sergenti is an invalid name taxonomically as it has been used to previously describe a parasite of sheep (Morel and Uilenberg 1981). In 1985 it was suggested that this group of Theileria parasites are the same species, based on serological and morphological identities, and it was
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pathological effects through erythrocyte destruction (Eamens et al. 2013c), and include T.
proposed T. orientalis be used to name the group (Uilenberg 1985).
Molecular studies, in the form of major piroplasm surface protein (MPSP) gene sequencing, have been used as a practical means of classification, as the strain types correlate with virulence. Based on molecular studies, MPSP and 18S rDNA sequences, the T. sergenti/T. buffeli/ T. orientalis group
of Theileria parasites can be designated as one group (Kamau et al. 2011; Sivakumar et al. 2014), hereafter known simply as T. orientalis. Within this species four major MPSP types were initially identified; p32 (Type 5), Buffeli, Chitose and Ikeda, with the latter being strongly associated with clinical disease in Australia, Japan and 2
New Zealand (Eamens et al. 2013c). Further phylogenetic analysis of the T. orientalis MPSP gene sequences revealed 11 allelic types (Sivakumar et al. 2014).
Life cycle and pathogenesis The genus Theileria comprises tick-transmitted protozoa characterised by schizonts in lymphoid cells and piroplasms in red blood cells of the vertebrate host. Transmission of T. orientalis occurs through the feeding of infected ticks of the Haemaphysalis genus (Riek 1982; Stewart 1987). New Zealand has only one livestock-infesting tick present, H. longicornis (Heath 2015), and this is
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considered to be the vector of T. orientalis in this country (McFadden et al. 2011). Ticks are infected while feeding on an infected host whose erythrocytes contain Theileria spp. piroplasms. The ingested erythrocytes are lysed in the gut lumen. A proportion of the released
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spherical zygote results, which invades a gut epithelial cell. The parasite then undergoes meiotic division and differentiates into a motile kinete. During or just after the tick moults to the next instar
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the kinete escapes from the gut cell and gains access to the haemocoel. It then migrates to the salivary glands and invades a specific population of salivary gland cells. It is in the salivary glands where the only multiplication stage of the parasite in the tick occurs (sporogony) and the parasite develops into a multinucleate sporont (Shaw 2002). Sporozoite development occurs during tick
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mammalian host (Shaw 2002).
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feeding and results in many thousands of sporozoites, which are released slowly into the
Transstadial transmission but not transovarial transmission occurs in ticks (Stewart et al. 1996). There is also a possibility that transmission could occur due to biting flies (Stomoxys calcitrans) and
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sucking lice (Linognathus vituli), or via vaccination needles(Fujisaki et al. 1993), but the life cycle is not maintained in lice or flies. The infected ticks transmit the infective sporozoite stage in their saliva as they feed. The
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piroplasms differentiate into gametocytes and fertilisation (syngamy) occurs in the gut lumen. A
sporozoites then invade leucocytes and within a few days develop into schizonts. In a study on H.
longicornis recovered from a paddock where infected cattle were grazing in Japan, about 20% were
found to have T. orientalis in their salivary glands (Kamio et al. 1990). At approximately 10 days post inoculation with sporozoites, schizonts can be detected transiently in the lymph nodes, spleen and liver. Schizont-infected cells are not usually found in the peripheral blood and the schizont does not appear to play a major role in pathogenesis (Sugimoto and Fujisaki 2002).
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The lymphoid life stage of T. orientalis (Buffeli) has been demonstrated by Stewart et al. (1988). After experimental infection of cattle, macroschizonts were demonstrated in Giemsa-stained lymph node preparations for between 6 and 20 days following tick infestation. The presence of schizonts was confirmed by immunofluorescence with sera from known infected animals. Microschizonts were seen infrequently. Piroplasms can be detected in the erythrocytes at approximately 10 days post inoculation. At this time transient pyrexia may also be observed in addition to the development of anaemia. In immunologically exposed animals there is generally a low level of parasitaemia (Shimizu et al.
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1992). Animals do recover from the infection although the parasites may persist, possibly for life. Consequently, relapses can occur during times of stress such as pregnancy, lactation or rapid
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changes in environmental conditions (Sugimoto and Fujisaki 2002).
erythrocytes (Kawamoto et al. 1990), but the pathogenesis of anaemia consequent to infection is not
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clearly established and may be multifaceted (Stockham et al. 2000). Studies of erythrocyte survival in infected calves demonstrated that both infected and uninfected erythrocytes have reduced survival (Yagi et al. 1991). An immune-mediated process for erythrocyte destruction has been suggested. However, other studies indicate that erythrocyte destruction can occur without immunoglobulin or complement involvement (Hagiwara et al. 1995). Shiono et al. (2001)
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demonstrated that the progress of anaemia is associated with elevated levels of methaemoglobin, a
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product of haemoglobin oxidation. An increase in methaemoglobin causes the release of superoxide radicals from haemoglobin which could possibly result in oxidative damage of erythrocytes and
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their removal from the circulation by the reticuloendothelial system (Sugimoto and Fujisaki 2002).
Clinical signs
Clinical signs of weakness, reluctance to walk and abortion are early but non-specific indications of
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Theileria orientalis exerts its major effect due to its piroplasmic form causing destruction of
infection with T. orientalis, particularly if accompanied by a history of cattle being moved. Physical
examination may reveal pallor (pale eyes, vaginal mucosa), pyrexia, and elevated heart and respiratory rates (Izzo et al. 2010). Blood samples in EDTA can be collected for laboratory analysis.
Thin smears under Giemsa stain show T. orientalis parasites in variable numbers of erythrocytes (0.5–30%). Packed cell volume can range from near normal down to 8% in severely-affected cases (Irwin 2013). The Buffeli type doesn’t appear to be associated with anaemia, however the Chitose and Ikeda types are associated with anaemia (Eamens et al. 2013c). In surveys of cattle in New South Wales, Queensland and Victorian, Chitose and Buffeli appear most commonly in non-clinical isolates, but may appear alongside Ikeda in clinically-affected animals (Eamens et al. 2013a). 4
Cattle are thought to become infected within three weeks of being placed on pasture harbouring infected vectors and begin to develop anaemia and related clinical signs soon after (Nakamura et al. 2010). Disease is more frequently seen when naive animals are introduced into an endemic area or when infected animals are introduced to a herd where a competent vector is present but Theileria species are not present or only at a low prevalence (Eamens et al. 2013a) It has been suggested that combined infections with different strains of T. orientalis may assist the parasite to sustain infection in the cattle host by presenting a variety of immune targets rather than a
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few (Eamens et al. 2013c).
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Diagnosis
Theileriosis can be diagnosed by light microscopic examination of dried Giemsa-stained blood
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be very low, in the order of 0.02–0.03% (Kamio et al. 1990; Shimizu et al. 1992). Small piroplasms of various shapes can be observed in the erythrocytes (Stockham et al. 2000). Erythrocyte infection al. 2010; McFadden et al. 2011).
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>1% and up to 30% are generally associated with severe anaemia and related clinical signs (Izzo et
Serological methods including ELISA to detect Theileria spp. antibodies in the blood of hosts was widely used in Japan for both diagnostic (Ota et al. 2009) and epidemiologic purposes (Minami et
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al. 1980). In one study, ELISA was found to be more sensitive than light microscopy for established
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infections, but the reverse was true for new infections, as seronegative/microscopy-positive cows checked 2 months later had seroconverted (Shimizu et al. 1992). Serology (indirect fluorescent antibody test) has also been used for survey work in Australia (Stewart et al. 1992).
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Specific diagnosis of theileriosis now relies on PCR assays to identify the MPSP (Kim et al. 1998). This method can detect infection in cattle 2 weeks before infected erythrocytes are visible by light microscopy (Ota et al. 2009) and also allows differentiation of different MPSP types that may be
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smears (Biddle et al. 2013). In infected but non-clinically-affected cattle erythrocyte invasion may
associated with pathogenicity or geographic specificity (Kubota et al. 1996; Kim et al. 2004). Refinement of PCR methods has resulted in highly sensitive and specific tests including the
multiplexed tandem PCR (Perera et al. 2015).
Bovine theileriosis in New Zealand The first published report of T. orientalis in New Zealand was in 1984 (James et al. 1984), and explained that the occurrence of this parasite in New Zealand was unsurprising, as at that time cattle were imported from Britain and Australia where the parasite was known to occur. Despite the parasite not being identified in New Zealand prior to this time it was likely to already have been 5
present for several years. The reason it remained undetected until that point is open to conjecture (James et al. 1984). Following the first description of T. orientalis in New Zealand, the number of reported cases increased until 1985 when the Whangarei Animal Health Laboratory diagnosed 60 cases or outbreaks, with the most common presenting signs being ill thrift, drop in milk and meat production, anorexia, malaise, depression, and diarrhoea. This disease then disappeared before reemerging 4 years later in Wairoa and Northland. It was suggested that T. orientalis was widespread in New Zealand and when environmental conditions are appropriate for the multiplication of ticks,
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and when susceptible animals are present, the disease appears (Thompson 1991).
Rawdon et al. (2006) described the investigation of jaundice, pyrexia, collapse, and death in a 20-
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month-old steer from north Waikato. Examination of blood smears from this individual revealed other causes of haemolytic anaemia and concluded that T. orientalis was the responsible agent and
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the primary cause of death.
In 2009 one outbreak of anaemia associated with infection by Type 1 (Chitose) strain of T. orientalis in a group of cattle moved from South Otago to Northland was described as affecting 38% of investigated animals with 1% mortality (McFadden et al. 2011). This investigation concluded that members of the T. orientalis group present in New Zealand were capable of causing
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disease in cattle not necessarily debilitated by another disease. In December 2012, the Ministry for Primary Industries’ Animal Health Laboratory first identified T. orientalis Ikeda, which had not previously been identified in New Zealand. Since late 2012
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outbreaks of anaemia associated with T. orientalis Ikeda have been reported in dairy and beef cattle herds located in multiple regions (Northland, Auckland, Waikato, Taranaki, Manawatu/Wanganui, Bay of Plenty and Wellington). Outside the known endemic tick areas the impact of the disease
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over 50% of erythrocytes to be parasitised with T. orientalis. The authors of this study ruled out
appears to be much less severe. The number of outbreaks in cattle herds has steadily increased since T. orientalis Ikeda was first identified in New Zealand (McFadden et al. 2013). In the early stages of the epidemic, genotyping of T. orientalis from these outbreaks was carried out and one was identified as T. orientalis Ikeda strain. Other strains present were T. orientalis Chitose and T. orientalis Buffeli. The Ikeda strain reportedly has greater pathogenicity than other endemic strains present in New Zealand (Chitose and buffeli) (McFadden et al. 2013).
6
It is not possible to say how long the Ikeda strain has been present in New Zealand. Testing of stored serum samples for T. orientalis organisms, prior to December 2012, from investigations from Northland collected since 2008 failed to detect the Ikeda strain (McFadden et al. 2013).
Bovine theileriosis in Australia Infection of cattle in Australia with T. orientalis was first recorded in 1910 (Seddon and Albiston 1966). Distribution is widespread, with herd and individual animal seroprevalence in Queensland of 75% and 41% respectively (Stewart et al. 1992). Infection has also been detected in cattle across
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solitary location in southwest Western Australia (Anonymous 2014).
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New South Wales (Eamens et al. 2013b), eastern and northern Victoria (Perera et al. 2013) and in a
Until the mid-2000s infection was considered benign (Mahoney 1994) with only occasional reports
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Wales with increasing frequency from 2006–2010 (Izzo et al. 2010) with the number of clinical cases climbing until 2013 (Eamens et al. 2013b). In 2008 there were 52 reported cases of clinical
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theileriosis in New South Wales alone, accounting for an estimated 800 deaths (Paul Freeman,1 pers. comm.). In a population of 460 cattle on 46 randomly-selected beef farms in the New England district of New South Wales, 110 (22% ) cattle and 33 (72%) properties were found to be positive on light microscopy (Biddle et al. 2013). In Victoria, occasional cases had been observed
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historically, but the first confirmed case with the Ikeda strain was seen in 2011 (Islam et al. 2011),
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with dozens of cases since reported.
Fundamental research was conducted on theileriosis by the Wacol Tick Fever Centre in the 1980s, due to incidental infection with what was then known as T. buffeli causing contamination of the live
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tick fever (Babesia/Anaplasma) vaccine. As a result, effective means were devised for treating infected calves prior to them becoming vaccine donors, along with the clarification of the parasite’s epidemiological features (Stewart et al. 1988, 1990a).
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of clinical disease (Rogers and Callow 1966). Clinical theileriosis was reported in New South
Genotypes of T. orientalis in Australia
Theileria orientalis found in Australia was, until recently, described as T. buffeli (Gubbels et al. 2000). The species is now accepted to be T. orientalis, the same as that found in East Asia. Buffeli is now used as a descriptor of the strain found mainly in benign cases, rather than as a species name. Historically, typing showed serological differences (detected by ELISA) between Australian isolates and those from Japan and Britain (Kawazu et al. 1992). Queensland (Warwick) isolates of T. orientalis were identified as T. buffeli and further evidence for them to be considered separate 1P
Freeman, NSW DPI, Wollongbar, Australia
7
biologically was provided by the fact that transmission was possible in Australian marsupial ticks found in Queensland and northern New South Wales, but not H. longicornis (Stewart et al. 1996). Analysis of MPSP by PCR in 1995 revealed that Australian isolates showed proteins characteristic for Buffeli and Chitose, but not the Ikeda type often associated with virulence in Japan and other Asian countries (Kubota et al. 1996). In 2011 the first evidence was provided that the Ikeda strain was present and associated with virulent disease in New South Wales cattle (Kamau et al. 2011). This was confirmed separately in New South Wales (Eamens et al. 2013a) and Victoria (Islam et al. 2011). While Buffeli is the dominant strain found in Queensland, in Victoria it was only isolated
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from 2.4% of 213 cattle tested. In contrast, Ikeda was isolated from 91.1% of these cattle (Perera et al. 2013). Mixed infection with two or more strains is common and there may be antigenic drift
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within an isolate.
Until the 1980s T. orientalis in Australia was thought to be spread by the cattle tick Rhipicephalus
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(Boophilus) australis (formerly B. microplus). However transmission studies using H. longicornis and H. bancrofti showed that these two species were capable of transmitting T. orientalis, while B. microplus, Ixodes holocyclus and Amblyomma triguttatum were not (Riek 1982). However, in Queensland the T. buffeli life cycle was shown to involve either of two species of
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native tick, H. bancrofti and H. humerosa, but not H. longicornis (Stewart 1987). In southern New South Wales and Victoria, where H. bancrofti and H. humerosa are rare or non-existent, the vector
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is assumed to be H. longicornis. Strain differences were shown experimentally to affect vector transmissibility, in that Australian H. longicornis could only transmit T. sergenti and could not
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transmit Australian T. buffeli, while Japanese H. longicornis could transmit both (Fujisaki 1992). Further transmission studies need to be conducted on recent isolates of T. orientalis from Australia, including Chitose and Ikeda strains, to confirm transmissibility differences.
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Vectors of T. orientalis in Australia
The Australian strain of H. longicornis is assumed to originate from northern Japan, due to its parthenogenetic nature (Hoogstraal et al. 1968; Herrin and Oliver 1974). This species is distributed
widely across temperate Eastern Australia, as far south as East Gippsland and the Murray Valley in Victoria and north to Gayndah in Queensland. It has also been isolated from inland sites such as Tenterfield and Young, New South Wales (Roberts 1962), and in Western Australia. Although primarily considered a cattle tick, it commonly infests many other species. In Australia it has been isolated from horses, sheep, cats, dogs and pigs, as well as native animals such as the wallaroo (Macropus robustus) and bandicoot (Isoodon macrourus) (Roberts 1962). 8
Other vectors of theileriosis such as March flies (Tabanidae), mosquitoes or sucking lice have been suggested, as disease outbreaks have occurred without ticks being observed (Islam et al. 2011; Bailey 2013b; Irwin 2013). However, due to their three-host life cycle, Haemaphysalis spp. may infest cattle in low numbers without being obvious to the herd manager (Perera et al. 2013). In Japan, H. longicornis is considered to be the main biological vector of T. orientalis, but it is also transmitted mechanically by sucking lice (Fujisaki et al. 1993) and blood-feeding midges (Ceratopogonidae) (Onoe et al. 1994). This raises the possibility of mechanical transmission in Australia, either by arthropod vectors or via fomites such as vaccination needles, eartag pliers or
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rectal examination gloves. Nevertheless, studies have show that observation of ticks is correlated with detection of T. orientalis. (Burney and Lugton 2010), and treatment of cattle for ticks was associated with a lower detection of T. orientalis compared to farms that did not treat (Biddle et al.
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Epidemiology of T. orientalis in Australia
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Cattle movement is a prominent feature of the cases of T. orientalis infection reported in 2006– 2012. Many of the outbreaks of clinical disease in 2006–2010 were associated with cattle that had been moved to the coast from drier inland areas (Izzo et al. 2010). Foci of cases were initially seen in coastal New South Wales, (Burney and Lugton 2010) but reports of cases in inland areas after introduction of coastal cattle were typical of the second phase of the outbreak (Bailey 2011). Cases
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occurred in inland areas where none had previously been recorded and ticks were either not noted or
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considered rare. For example, cows on the point of calving in a herd of 122 cattle brought from Tasmania (and therefore presumed to be naïve) began to shown signs of theileriosis including 10
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deaths on arrival on farm at Moree, in inland northwest New South Wales (Irwin 2013). More recently, severe morbidity and high mortality has been noted in calves 6–14 weeks of age, especially on properties where theileriosis has previously been diagnosed in adult cattle (Ball 2013; Eastwood 2013). The economic cost of theileriosis outbreaks in Australia has been assessed by
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2013).
Perera et al. (2013, 2014).
Treatment and control
Attempts have been made to treat bovine theileriosis with imidocarb, oxytetracyclines and halofuginone, with equivocal results. Under research conditions, combinations of primaquine and buparvaquone, or primaquine with halofuginone totally eliminated infection of T. buffeli from splenectomised calves (Stewart et al. 1990b). In other countries buparvaquone alone has been used with success (Ozawa et al. 1988). However these products are either unavailable in Australia 9
(primaquine and buparvaquone) or in a formulation unsuitable for economical treatment of adult cattle (halofuginone). Trials on artificially-infected splenectomised calves showed that buparvaquone at a dose rate of 2.5 mg/kg injected once I/M was an adequate treatment for Buffeli, Chitose and Ikeda variants of T. orientalis (Carter 2011). However, tissue depletion studies for buparvaquone in cattle, conducted so that it could be used under permit in clinically-affected cattle in Australia, found that residues were present as long as 147 days after administration (Bailey 2013a). This is the main reason why
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buparvaquone is not used to treat cases in Australia.
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A noted above, tick control has been linked with a lower detection of T. orientalis. The only
products registered in Australia for control of H. longicornis are short-acting dips and sprays
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containing deltamethrin and ethion in combination, amitraz, chlorphenvinphos and cypermethrin in to 10 days. Flumethrin pour-on formulation is not available to treat cattle in Australia (Ottaway and
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Cook 2005). Because of this many veterinarians are recommending the off-label use of pour-on or injectable macrocyclic lactone products in the hope of providing longer protection for cattle on introduction to suspected danger areas.
Bovine theileriosis in Japan
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Theileriosis is recognised wherever cattle are found across the entire Japanese archipelago. The
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dominant species is currently referred to as T. orientalis, with most references prior to 2005 naming it as T. sergenti (Fujisaki 1992). It is now accepted that these names, as well as T. buffeli, all describe the same species (Uilenberg 2011) which can be characterised using molecular techniques
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targeting the MPSP antigens.
Vectors of T. orientalis in Japan
The main vector, H. longicornis (Itagaki and Ohishi 1990), is commonly isolated from cattle but
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combination, as well as flumethrin spray (aqueous solution) which has a period of protection of up
also infests dogs and other mammalian and bird species (Shimada et al. 2003). A characteristic of H. longicornis in Japan is that north of Tokyo mostly females are found and reproduction is thought to be through parthenogenesis, while in warmer southern areas males and females are found and reproduction is sexual (Itagaki and Ohishi 1990). In the southern islands of Okinawa the vector is H. mageshimaensis (Zakimi et al. 2006). Infection is also thought to be transferred mechanically, either by vectors such as tabanids or sucking lice, or alternatively by transplacental infection of calves (Onoe et al. 1994). New strains of T. orientalis are thought to have been introduced into Japan from Australia with imported cattle in the 1990s (Kawazu et al. 1995). A recent study using 10
PCR to isolate T. orientalis DNA from ticks collected in Okinawa and Hokkaido has shown that other H. megaspinosa and H. douglasi, as well as two species of Ixodes, are potential vectors (Yokoyama et al. 2012) Epidemiology of theileriosis in Japan
Clinical disease is reported as being seen mainly in dairy cattle in summer and autumn, usually associated with grazing on pasture, with a possible role of wildlife hosts contaminating pastures with infected ticks (Nishino et al. 2008). However, disease is also seen in confined cattle (Shimizu et al. 1992). Beef cattle, particularly the indigenous Wagyu breed, are considered less susceptible to
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infection (Higuchi et al. 1997). Groups of grazing Holstein heifers were monitored in a national study of 85 herds across 30 of Japan’s 50 prefectures. The incidence of infection and number of
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heifers requiring treatment were highest in southern regions (41.1% and 38.6%) and lowest in 2001).
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Treatment
As stress due to pregnancy, exercise or concurrent nutritional challenge was found to be a contributor to the expression of clinical theileriosis, supportive therapy including I/V fluids, nutritional supplements, and blood transfusion may be used. Iron dextran solution injected I/M over
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3 days was also found to aid recovery from infection (Nakamura et al. 2010).
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Primaquine phosphate and pamaquine were widely used against T. orientalis in the 1970s and 1980s. However, the efficacy of these two compounds under field conditions in Japan declined (Minami et al. 1985) leading to clinicians stopping their use. Buparvaquone has been successfully
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trialled on clinical cases in Japan but not registered (Ozawa et al. 1988). Tetrocarcin was also found to be effective in reducing parasitaemia but not registered (Ohtomo et al. 1985), while imidocarb was not found to be useful in treating infections (Minami et al. 1985).
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northern regions (18% and 6.2%), in proportion to observed tick numbers on cattle (Yamane et al.
Use of a live vaccine based on piroplasms was terminated due to the accidental transmission of potential pathogens including bovine leukaemia virus (Onuma et al. 1998). This led to attempts to create a subunit vaccine (Onuma et al. 1997). This has remained elusive to date, but studies on the T. orientalis genome to find a target site are continuing (Hayashida et al. 2012). As a preventive measure, attention has turned to tick control. Cattle are routinely treated with long-acting preparations of synthetic pyrethroids prior to putting out to graze on pasture, a strategy that has proved effective in reducing tick numbers and incidence of infection (Shimizu et al. 2000).
Conclusion 11
Theileria orientalis is an economically important parasite of cattle in New Zealand, Australia and Japan, especially where naïve animals are introduced into an endemic area or in animals under stress. Awareness of the risks posed by the parasite is required to enable management practices to be implemented to minimise its impact. Management of the tick vector may reduce the incidence of the disease, as will reducing stress on stock.
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Submitted 01 September 2014
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Accepted for publication 27 May 2015
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First published online [insert date]
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