Non-pathogenic Theileria species in cattle

Non-pathogenic Theileria species in cattle

Current Authors:
J A LAWRENCE - Extraordinary Professor, DPhil, BSc, MRCVS (ret.), DTVM, Department of Paraclinical Veterinary Science, University of Zimbabwe, Harare, Zimbabwe 
C BYARUHANGA - Post-doc Fellow, BVM, MVPM, PhD, Department of Veterinary Tropical Diseases, Para-clinical Building, Faculty of Veterinary Science, University of Pretoria, 100 Old Soutpan Road, Onderstepoort, Pretoria, Gauteng, 0110, South Africa
M OOSTHUIZEN - Parasitology, PhD, Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, Private Bag X04, University of Pretoria, Pretoria, Gauteng, 0110, South Africa
B J MANS - Principal Researcher, BSc, BSc (Hons) Biochemistry, MSc (Biochemistry), PhD (Biochemistry), Agricultural Research Council, Onderstepoort Veterinary Research, 100 Old Soutpan Road, Pretoria, Gauteng, 0110, South Africa

Introduction

A number of species of Theileria occur in cattle without causing disease. Theileria taurotragi, T. mutans and T. buffeli/orientalis most commonly cause inapparent to mild diseases and only occasionally result in more severe disease. Other species that have been identified without ever having been implicated in disease in cattle are:

  • Theileria taurotragi clade - Theileria sp.(bougasvlei), Theileria sp. (buffalo)
  • Theileria velifera clade - Theileria velifera, Theileria velifera A, Theileria velifera B, Theileria sp. RR-2012
  • Antelope clade - Theileria sp. (sable), Theileria sp. (sable-like) – infectivity for cattle doubtful
  • Theileria buffeli clade - Theileria sinensis, Theileria sinensis-like, Theileria sp. RMP-2013

The T. taurotragi clade is mostly composed of pathogenic Theileria, namely T. annulata, T. lestoquardi, T. parva and T. taurotragi (see Introduction Theilerioses of cattle). However, two more species are found in this clade that have to date not been associated with clinical disease, namely T. sp. (buffalo) and T. sp. (bougasvlei) 21, 22 These genotypes are unique species in their own right based on 18S, Cytochrome oxidase I (COI) and S5 ribosomal gene analysis 21, 34 but they have not been given appropriate species names as their tick vectors remain unknown and their complete life cycles have not been elucidated. 
Theileria velifera was first described 40 in Madagascar, under the name Haematoxenus veliferus, as a benign parasite of cattle characterized by the presence of a veil-like structure associated with intra-erythrocytic piroplasms (Figure 1). The parasite is widespread in eastern and southern Africa and also occurs in the Caribbean. It has no practical significance other than its role in confusing the diagnosis of Theileria parva. The parasite also infects African buffalo (Syncerus caffer). 36 Ancestral relationships have shown that the T. velifera clade is composed of four genotypes, T. velifera, T. velifera A, T. velifera B and Theileria sp. RR-2012, a yet undescribed genotype from cattle in India. 22 Whereas T. velifera B has only been reported in African buffalo, T. velifera and T. velifera A have been found in cattle and African buffalo. 7, 8, 21, 22

Theileria sp. (sable) causes mortality in naïve roan antelope (Hippotragus equinus) and sable antelope (Hippotragus niger) and presented as a lymphoproliferative condition in these antelope. 28 Transformed schizonts of T. sp. (sable) can be maintained in cell culture similarly to T. parva and T. sp. (buffalo). 50  Sable and roan antelope are considered the natural carrier host but identical genotypes based on the 18S rRNA genes have been found in dogs. 24 Reverse line blot has also indicated the extensive presence of T. sp. (sable) in cattle, African buffalo, blesbuck (Damaliscus pygargus), blue wildebeest (Connochaetes taurinus), klipspringer (Oreotragus oreotragus), reedbuck (Redunca arundinum) and nyala (Tragelaphus angasii). 1, 27, 28, 32, 47 A closely related genotype, T. sp. (sable-like) that differs by 6 base pairs in the V4 hypervariable region of the 18S rRNA gene has been described in a single ox in South Africa that presented with clinical signs of theileriosis, with high schizont parasitaemia and lymphoid infiltration of organs. 21 However, subsequent screening of cattle from South Africa using sequencing of the 18S rRNA gene failed to detect either T. sp. (sable) or T. sp. (sable-like). 23 Potential cross-reactivity with T. velifera in the reverse line blot probe has been considered as a possible explanation for this discrepancy.21

Theileria sinensis was first described in cattle in China based on infectivity studies, morphological observations and its inability to be transmitted by Hyalomma detritum and Haemaphysalis longicornis, the vectors of T. annulata and T. sergenti respectively. 4, 5 It was assigned to the T. buffeli/orientalis clade after molecular analysis and was named T. sinensis after classic taxonomic and molecular studies. 15 Molecular analysis based on the ITS1, ITS2 and 5.8S rRNA genes clearly differentiate it from T. sergenti and other members of the T. buffeli/orientalis clade, supporting its designation as a unique species in this clade. 18 A genotype and a possible new species, T. sinensis-like, that is closely related to T. sinensis, has been described in African buffalo in South Africa. 21 Screening of cattle and African buffalo using next-generation sequencing of the 18S rRNA gene indicated that this species is only found in buffalo. 23 A number of as yet undescribed genotypes  in the T. buffeli/orientalis clade also occur  in cattle, Nilgai (Boselaphus tragocamelus) and Asian buffalo in China and India, all designated as T. sp. RMP-2013. 22

Aetiology and life cycle

Theileria velifera has most likely a typical theilerial life cycle (see East Coast fever: Figure 29.2) but no detailed studies have yet been done. The parasite is transmitted by ticks of the genus Amblyomma, namely A. variegatum, 42 A. hebraeum, A. lepidum and A. astrion. 41The development of T. velifera in the gut and haemolymph of A. variegatum is typical of the Theileria genus 45 and the piroplasms are similar to those of Theileria mutans except that some are associated with the presence of a veil-like structure in the cytoplasm of the erythrocyte (Figure 1). This structure is believed to be composed of a crystalline derivative of haemoglobin. 43 Schizonts have not been described. The piroplasms are readily transmitted by inoculation of infected blood. 40

The life cycle, including the tick vectors, of Theileria sp. (buffalo) and T. sp. (bougasvlei) remains obscure, beyond the ability to transform schizonts. Levels of parasitaemia in African buffalo are similar to those observed for T. parva. 33, 34 Rhipicephalus appendiculatus and R. evertsi evertsi have been implicated as vectors of T. sp. (sable). 38 Theileria sinensis is transmitted by Haemaphysalis quinghaiensis and infects cattle and yaks (Bos grunniens). 46 Transmission by infected blood inoculation indicated that the parasites multiply prolifically in the erythrocytic stage. 5 Piroplasms are polymorphic with shapes that range from pyriform or circular to rod-shaped and some may exhibit bars and veils similar to other members of this clade.5  It is expected that its general life cycle will resemble other members of the T. buffeli/orientalis clade.

Epidemiology

Little is known of the epidemiology of T. velifera. It is assumed to be widespread throughout the range of its tick vectors. Theileria velifera infections were detected in cattle in Uganda, 3, 7, 25, 29, 31 Kenya, 27 Nigeria 20 and South Africa, 21 and in African buffalo in Uganda, 30, 31 Botswana 12 and South Africa. 8 21 The prevalence of T. velifera may reach 100 per cent, depending on location and ecology, 3, 30, 31 The protective effect of T. velifera co-infection against T. parva infection is discussed Theileria mutans infection.
Theileria sp. (buffalo) has been detected in African buffalo in Botswana, Kenya, Mozambique, Uganda, South Africa and Zimbabwe.8, 12, 21, 23, 34 It was first distinguished from T. parva due to differences observed in antigenicity using monoclonal antibody panels 11 and was shown to have a unique 18S rRNA sequence. 2 Theileria sp. (buffalo) was successfully cultivated in cell culture as schizonts from an African buffalo that showed patent Theileria schizont and a 10 per cent piroplasm parasitaemia.49 Most studies that screened cattle for Theileria parasites found no evidence of this parasite, while African buffalo showed a high prevalence (50-100 per cent). 21, 23, 30, 34, 47 However, recently the presence of T. sp. (buffalo) was detected in 67 per cent of cattle grazing with buffalo in Marula, a private ranching farm in Nakuru, Rift Valley in Kenya. 13 It was also showed that T. sp. (buffalo) could transform cattle-derived lymphocytes. 6  Whether this parasite plays a role in clinical theileriosis in cattle has not yet been established, but results thus far suggest that it is not transmissible between cattle. 6 Theileria sp. (bougasvlei) has been detected in Botswana, Mozambique, Namibia, South Africa and Zimbabwe.23  Studies of the distribution of T. sp. (buffalo) and T. sp. (bougasvlei) demonstrated an apparent antagonistic behaviour, in that buffalo herds or farms are almost exclusively infected by either one or the other, even in regions of sympatry such as the Kruger National Park in South Africa. 23, 34 This was interpreted as potential hybrid sterility that allowed speciation while still using the same tick vector and carrier host. 34

Theileria sp. (sable) has been detected in a variety of hosts using reverse line blot in South Africa as indicated above. It has also been detected in Nigeria 1and Kenya. 27 Its tick vectors, R. appendiculatus and R. evertsi occur from southern Africa to East Africa,44 and mortality in roan and sable antelope has been recorded in Swaziland and Zimbabwe.
Theileria sinensis has been detected mainly in China in cattle and yaks. 16, 35  A study that focused on piroplasms in dogs in the Gansu province of China found 6.4 per cent of animals sampled positive for T. sinensis. 26Theileria sinensis or a very closely related genotype was also detected in Asian buffalo in the Amazon region of Brazil. 37

Clinical Signs

No clinical signs have been recorded for T. velifera in intact infected animals. Anaemia has been described in infected splenectomized calves.42

Pathogenesis and pathology

No studies have been undertaken on the pathogenesis or pathology of T. velifera infection. There is currently no evidence that T. sp. (buffalo), T. sp. (bougasvlei), Theileria sp. (sable) or Theileria sinensis are pathogenic in cattle.

Diagnosis and differential diagnosis

Real-time PCR assays specific for T. sp. (buffalo) and T. sp. (bougasvlei) have been developed. 34 These are useful to differentiate and confirm mixed infection with T. parva, to estimate parasitaemia in carrier animals and to determine the geographic distribution of these parasites. A real-time PCR assay that can differentiate Theileria sp. (sable) and T. sp. (sable-like) has been developed and is being validated. 22

Theileria velifera infection can be differentiated from other benign theilerioses if piroplasms associated with veil-like structures are found in erythrocytes. However, as yet, no serological test or species-specific monoclonal antibodies are available. The RLB hybridisation assay was developed to detect T. velifera and other Theileria species, using species-specific probes. This was based on the assumption that the 18S hyper-variable region is conserved within species. 44 However, significant similarity exists between the RLB probe for Theileria sp. (sable) and T. velifera, resulting in the reporting of a relatively high prevalence (40-50  per cent) of Theileria sp. (sable) in cattle and African buffalo 12, 28, 47 that may be attributable to the presence of T. velifera. 21 Further, the RLB assay does not detect variations in the 18S rRNA gene sequences of T. velifera, 9 and therefore, the assay has to be validated when screening novel vertebrate species or animals from different geographical locations.

An ELISA has been developed based on the recombinant major piroplasm surface protein of T. sinensis. 48  Significant cross-reactivity with positive sera for T. annulata and T. orientalis were found, making the use of this assay for epidemiological surveys limited where these species share similar geographical distributions. Conventional PCR assays capable of distinguishing T. sergenti and T. sinensis in cattle and yaks have been developed based on the major piroplasm surface protein. 17 A LAMP PCR assay was also developed for the same purpose based on ITS sequences. 18, 19 A PCR-RFLP assay that targets the RPS8 gene can distinguish between T. annulata, T. sinensis, T. sergenti, Babesia ovata, B. bovis, B. bigemina,and B. major and Babesia species Kashi isolate, the major piroplasms of cattle in China. 39

Control

As T. velifera is a benign parasite, there are no indications for its treatment or control. The same applies for T. sp. (buffalo) and T. sp. (bougasvlei). In the case of T. sp. (sable), buparvaquone was successful in treatment of clinical theileriosis in roan and sable antelope. 38

Figure 1 Line drawing of piroplasms of Theileria spp. which develop veils

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