Theileria buffeli/orientalis infection

Previous Authors: J A LAWRENCE

Current Authors:
J A LAWRENCE - Extraordinary Professor, DPhil, BSc, MRCVS (ret.), DTVM, Department of Paraclinical Veterinary Science, University of Zimbabwe, Harare, Zimbabwe  
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

GENERAL INTRODUCTION: THEILERIOSES OF CATTLE

Introduction

The Theileria buffeli/orientalis group of parasites is widely distributed in cattle around the world. The taxonomy of the group is complex and the nomenclature controversial. The name T. buffeli was given to a parasite recovered from Asiatic buffalo in Indochina by Neveu-Lemaire in 1912, and that of T. orientalis to a parasite recovered from cattle in Siberia by Yakimoff and Soudatschenkoff in 1931.²⁰ The name Theileria sergenti is frequently used to describe a pathogenic member of the T. buffeli/orientalis group that occurs in eastern Asia, but this name is invalid as it had been used previously to describe a parasite of sheep.²⁰ The group also contains other known species such as T. sinensis found in Asia and T. sp. (kudu) found in Africa ¹⁶.  Uilenberg proposed in 1985 that the group be named T. orientalis, while later authors proposed T. buffeli, but no consensus has been reached. Both names are used synonymously, depending on the historical background of different scientific groups ¹⁶.

The parasites have been described from Asia, Australasia, the Mediterranean basin, Western Europe and North America, although they have often been identified mistakenly as Theileria mutans. Under the name T. orientalis the parasites were first identified in sub-Saharan Africa in Ethiopia in 1983² and they have since been described in central Africa¹³ and eastern Africa, where they were initially named Theileria sp. (Marula).²¹ The parasites have also been identified in African buffalo (Syncerus caffer) in South Africa¹. In most parts of the world the parasites are usually benign, or cause only mild clinical signs, but in eastern Asia, Australia and New Zealand they may pose an economically significant threat to cattle production.

Sequencing of the 18S rRNA gene has identified 13 different genotypes for the group ^{5, 16, 17, 18}.  A number of major piroplasm surface protein (MPSP) types have been identified, including Buffeli, Chitose, Ikeda and Warwick.   One of these, Ikeda, is responsible for clinical disease in Japan, Australia and New Zealand. In southern Africa the T. buffeli that are found in cattle and buffalo belong to different genotypes, which raises the possibility that they may represent different species ¹⁸.

Aetiology, life cycle and epidemiology

The parasites in the T. buffeli/orientalis group normally infect cattle, Asiatic domestic buffalo and African buffalo. Infection in sheep has been detected by molecular methods in China and Vietnam. The morphological and biological characteristics of the group are similar to those of Theileria parva (see East Coast fever: Figure 29.2). Schizonts may be found briefly about 10 days post-infection, and piroplasms appear at the same time.  The macroschizonts are unusually large.²⁹ The piroplasms are often longer than those of other species, and bars are usually found in the erythrocytes associated with the piroplasms; veils are also commonly found with certain isolates, but not with others.^{13, 21, 29}

The main vectors of the group are Haemaphysalis punctata in Europe, the Mediterranean basin and western Asia, H. longicornis, H. japonica and H. concinna in eastern Asia,²⁸ H. humerosa and H. bancrofti in Australia,²⁴ and H. longicornis in Australia and New Zealand.  Peak incidence of infection coincides with peak activity of nymphal and adult ticks in spring and autumn respectively ¹⁹.  In Japan, H. longicornis is considered to be the main vector, but the parasite is also transmitted mechanically by sucking lice and tabanid flies. Mechanical transmission with vaccination needles and other agents is possible, but the disease is usually associated with the presence of the vector ticks. The vectors in North America and sub-Saharan Africa have not been identified. No Haemaphysalis ticks occur on cattle in North America, while in Africa the only Haemaphysalis that occurs on cattle as both immatures and adults is H.aciculifer,²⁷ which is not thought to be sufficiently common to act as a vector.² It has been suggested that H. silacea may be the possible vector of buffalo specific members of this group in South Africa, since it was found to parasitize buffalo in some of the regions where parasites occur ^{5, 10,18,30}.  Ixodes species are possibly involved, as two species have been identified as potential vectors in Japan. The parasite is readily transmissible between cattle by blood inoculation.²⁹ Transplacental infection does occur in the field at a low rate but is not considered to be a major factor in the epidemiology of the disease ^{15, 25}.

The Theileria buffeli/orientalis group is assumed to be widespread throughout the range of its tick vectors and often occurs in mixed infections with other species of Theileria. It is rarely associated with clinical disease, except in cattle of exotic breeds in eastern Asia and in Australasia, where the Ikeda strain has been incriminated. Benign Theileria buffeli/orientalis infection with the Buffeli, Warwick and Chitose strains had been known to be endemic in Australasia from the early 1900’s, causing occasional outbreaks of disease characterized by anaemia with low mortality. The severity of the disease escalated with the appearance of the Ikeda strain in Australia in 2006 and in New Zealand probably 2-3 years ¹⁴; the source of the strain has not been identified. The disease assumed epidemic proportions in New Zealand in 2012. Export of cattle from Australia to Vietnam and Pakistan resulted in theileriosis outbreaks there that could be linked with the presence of T. buffeli (Ikeda) in the cattle ^{6, 8}.

Movement of infected cattle into areas in which the vector tick is present is the main method of spread ¹⁴. Outbreaks are usually associated with introduction of naïve cattle to infected farms; cattle usually become infected within three weeks of arrival ²⁶. On farms where the disease is endemic, most calves demonstrate evidence of infection by 3-6 weeks of age. Colostral antibodies appear not to confer protective immunity. The Ikeda strain usually occurs together with the less virulent strains, and previous infection with less virulent strains appears to provide no protection against Ikeda.

Clinical signs

The clinical signs of bovine theileriosis include lethargy, fever, anaemia, jaundice, and reduced milk production, with mortality in naïve herds as high as 5% ²⁵. Mortalities include still-born calves and late term abortions, the latter being a major feature of the disease. Young calves appear to be highly susceptible to theileriosis, with clinical anaemia and death in herds where the disease is endemic.  Infection is often subclinical, but once cattle are infected they appear to harbour the parasite long-term. Stress appears to be a major factor in precipitating disease, and therefore pregnant and recently calved cows are at high risk of developing clinical theileriosis.

Pathogenesis and pathology

The major effect of Theileria buffeli/orientalis is destruction of erythrocytes by the piroplasms, but the pathogenesis of anaemia consequent to infection is not clearly established and may be multifaceted.  Both infected and uninfected erythrocytes have reduced survival times, and an immune-mediated process for erythrocyte destruction has been suggested. However, other studies indicate that erythrocyte destruction can occur without immunoglobulin or complement involvement. The progress of anaemia is associated with elevated levels of methaemoglobin, a 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 their removal from the circulation by the reticuloendothelial system.

The most striking feature seen at necropsy is pallor of the carcase and an enlarged ochre-coloured liver with rounded margins ²⁶. The spleen is also enlarged. Histopathological changes are generally consistent with anaemia.

Diagnosis and differential diagnosis

Theileria buffeli/orientalis infection may be suspected when a febrile reaction and anaemia occurs in cattle exposed to Haemaphysalis infestation, and elongated piroplasms associated with intra-erythrocytic rods, and possibly with veils, are demonstrated in blood smears. Large schizonts may occasionally be demonstrated in lymph smears. As piroplasms may be found in the erythrocytes of healthy cattle, blood smear diagnosis is based on the confirmation of a regenerative anaemia together with the presence of organisms and the absence of other diseases that may cause anaemia in cattle ²⁶.  It is common for severely affected animals to have a packed cell volume (PCV) of less than 10%, and the percentage of erythrocytes that are parasitised can be extremely variable. Blood smears show anisocytosis with polychromasia and basophilic stippling. Howell-Jolly bodies and nucleated RBCs are also observed. Elevations in hepatic enzymes are frequently observed, presumably caused by hypoxia-induced hepatopathy.

Differentiation of infection with T. buffeli/orientalis from infection with other species of Theileria can be made by use of a variety of serological assays ¹⁶, including the piroplasm indirect fluorescent antibody test (IFAT), piroplasm extract enzyme-linked immunosorbent assay (ELISA), latex agglutination test for major piroplasm surface protein p33, an indirect ELISA for p33, and an ELISA based on the major piroplasm surface protein ³¹. ELISA using the major surface piroplasm proteins can distinguish between different strains of the group ¹².

Various molecular tests have been developed that can detect T. buffeli/orientalis genes ¹⁶. These include the reverse line blot (RLB); conventional PCR for β-tubulin, MPSP, p23, p32, p33, p34; a semi-nested PCR for 18S rRNA; a multiplexed tandem PCR assay based on the piroplasm surface protein p23 (Buffeli), major piroplasm surface protein MPSP (Chitose; type 5), and the first nuclear ribosomal internal transcribed spacer (ITS-1) (Ikeda) ^{7, 22}; real-time PCR ^{3, 9, 23}; and the LAMP PCR assay.

Control

As T. buffeli/orientalis is usually a benign parasite there are no indications for its treatment or control. Where it assumes a pathogenic characteristic, as in eastern Asia and Australasia, treatment with the antimalarials primaquine phosphate and pamaquine has proved effective at times. Imidocarb has given variable results. Buparvoquone is effective, but is not registered in those countries because of persistence of residues.

Where necessary, infection can be prevented by appropriate methods to limit exposure of susceptible cattle to infected ticks. It is common practice in eastern Asia to stimulate immunity to the parasites by deliberately exposing cattle to tick infestation and treating them prophylactically.³ No effective vaccine has been developed.

References

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