Life cycle of Theileria in cattle and tick vector

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CHAPTER 2 Literature Review

The genus Theileria is a group of obligate, intracellular, tick -transmitted, apicomplexan parasites that infect wild and domestic ruminants throughout the world (Allsopp et ai., 1993). Cattle and buffalo in Africa are usually co-infected with pathogenic, mildly pathogenic and non-pathogenic Theileria spp. These species are transmitted by different tick vectors and their geographical distribution depends on the distribution of their tick vectors.

Classification of Theileria spp.

Theileria parasites belong to the super-group Chromalveolata; phylum Apicomplexa (Adl et ai., 2005). Apicomplexan parasites are single celled eukaryotes with an apical complex in some of the life-cycle stages. Members of the family Theileridae (Theileria and Babesia) have schizont stages in lymphocytes. In Theileria, the piroplasm stages in erythrocytes lack a pigment (Irvin, 1987).

  • Classification: (Aql et ai., 2005)
  • Supergroup: Chromalveolata
  • Superphylum: Alveolata
  • Phylum: Apicomplexa
  • Class: Aconoidasida
  • Order: Piroplasmida
  • Family: Theileriidae
  • Genus: Theileria

Life cycle of Theileria in cattle and tick vector

The life cycle of Theileria parva is a typical apicomplexan life cycle (Figure 2.1) with an alternation of sexual and asexual stages that are found in the mammalian and tick host. Sporozoites are inoculated into the bovine host by the tick during a blood-meal. These enter lymphocytes and develop into schizonts. The lymphocytes are transformed and immortalized by the parasite. Schizonts stimulate the host cells to divide, and as cell divides, the schizont also divides, resulting in infection of the daughter cells. This synchronization of the division of host cells and schizonts results in the invasion of various host tissues by infected cells, causing a severe and sometimes fatal disease (Kaba et aI., 2005). Some of the schizonts develop into merozoites, which are then released into the bloodstream where they invade erythrocytes and transform into piroplasms which are the stages that are infective to the tick.
Inside the gut of the tick, the piroplasms differentiate into male (micro-) and female (macro-) gametes which then fuse to form a zygote. The zygote then enters gut epithelial cells and develops into akinete. Kinetes then emerge from the epithelial cells and migrate to the salivary glands of the tick where they transform into sporoblasts, each of which produces thousands of sporozoites. The cycle is then continued by inoculation of the sporozoites into the mammalian host by the tick.

Theileria species of buffalo and cattle in Africa

The most pathogenic (malignant) species of cattle are T. parva and Theileria annulata. These Theileria parasites are of major economic importance to the cattle industry due to high mortality and morbidity, cost of control and treatment, as well as loss in production by infected animals (Allsopp et aI., 1993; ILRAD, 1990; OlE 2000; McKeever, 2001; Schnittger et aI., 2002).
Theileria parva infects cattle and buffalo in eastern, central and southern Africa and is the causative agent of East Coast fever (ECF), January disease and Corridor disease in cattle (ILRAD, 1990; Gubbels et aI., 1999). Theileria parva is transmitted transstadially by the three-host ticks, Rhipicephalus appendiculatus, Rhipicephalus zambeziensis and Rhipicephalus duttoni (Young et aI., 1978b; Lawrence et aI., 1983; Norval et aI., 1992). The African buffalo (Syncerus cajJer) is the natural reservoir host of T. parva and infections in buffalo are usually asymptomatic, but are acute and usually fatal in cattle (Lawrence et aI., 1994c). The African buffalo is an indigenous bovine of sub-Saharan Africa and has lived in harmony with T. parva and its vector R. appendiculatus long before cattle were introduced into the region (Grootenhuis, 1988). Other reservoir hosts of T. parva are water buffalo (Bubalus bubalis) and waterbuck (Kobus defassa) (Stagg et aI., 1994; CFSPH, 2009).
Theileria annulata infects cattle, yak, water buffalo and camels in northern Africa, southern Europe, the Middle East and Central Asia where it causes tropical theileriosis (Sergent et aI., 1935)
Mildly pathogenic and benign species of Theileria that infect cattle and buffalo in Africa are Theileria mutans, Theileria velifera, Theileria bujJeli, Theileria taurotragi and Theileria sp. (buffalo) (Allsopp et aI., 1993; Gubbels et aI., 1999; Oura et aI., 2004). Theileria parasites usually occur as mixed infections in infected animals (Georges et aI., 2001) and although the benign and mildly pathogenic forms do not have any significant economic importance, they can interfere with the diagnosis of the pathogenic forms and therefore confuse their epidemiology (Lawrence et aI., 1994a).

Theileria parva (Theiler, 1904)

Theileria parva is transmitted by the three-host ixodid ticks, R. appendiculatus, R. zambeziensis and R. duttoni (Jongejan et aI., 1980; Lawrence et a!., 1983). It occurs in 11 countries in Africa, extending from southern Sudan to northern KwaZulu-Natal in South Africa (Figure 2.2). The African buffalo (Syncerus caffer) is the natural host of this parasite and infected buffalo usually remain long-term, asymptomatic carriers (ILRAD, 1990; Uilenberg, 1999). The parasite is the causative agent of ECF, January disease and Corridor disease in eastern, central and southern Africa (Collins et a!., 2002). These disease syndromes differ in their clinical symptoms, pathogenicity, epidemiology and host (cattle or buffalo) (Allsopp et aI., 1993).
Due to these differences, T parva was initially classified into three sub-species, namely T. parva parva, T parva bovis and T parva lawrencei. However, this classification was abandoned due to lack of molecular evidence as these sub-species are genetically similar (Norval et aI., 1992; Allsopp et aI., 1993). It has since been recommended that the different isolates should rather be classified as cattle- or buffalo-associated depending on the original host (Anon, 1989).

East Coast fever (ECF)

ECF is a fatal disease of cattle caused by cattle-associated T. parva (previously known as T. parva parva) (Lawrence et aI., 1994b). It is a major constraint to livestock production in Africa. Total annual losses due to ECF on the continent are estimated at around one million cattle and $168 million loss in revenue (Mukhebi et aI., 1992; Norval et aI., 1992). Twenty-four million cattle are at risk of infection (Norval et aI., 1992). The pathogenicity of T. parva is mainly due to transformation and proliferation of the host T -lymphocytes that is induced by the parasite during schizogony, resulting in lymphocytolysis, and usually death of the animal (Ebel et aI., 1997; Nene et aI., 2000). The clinical signs of ECF include fever, anorexia, decreased milk productions and nasal discharge (CFSPH, 2009). If untreated, death occurs within three to four weeks of infection (ILRAD, 1990). NaIve animals develop an acute infection, and if they survive, are able to mount an immune response that results in a carrier state with low levels of parasitaemia and disease (Beck et aI., 2009). These animals usually become asymptomatic carries and are therefore responsible for most of the transmission.

The epidemiology ofECF in southern Africa

The disease was introduced into southern Africa in early 1900 by importation of cattle from the East coast of Africa after the rinderpest epidemic (Norval et aI., 1992; Uilenberg, 1999). It was first reported in Zimbabwe in 1902 where it was introduced through a consignment of cattle brought from East Africa through Mozambique. The disease later spread to southern Zimbabwe and then southwards to Swaziland and neighbouring south-eastern Transvaal and Natal (now Mpumalanga and KwaZulu-Natal) provinces of South Africa until it reached the Cape of Good Hope (Cape Town) in 1910 (Norval et aI., 1992).
An estimated 5.5 million cattle died In South Africa due to ECF (Stoltsz, 1989). Due to its devastating effects in cattle, massive control strategies were implemented. These included clearing of infected pastures by removal of healthy cattle, intensive dipping and surveillance programmes, and mass slaughtering of infected cattle. This led to the total eradication of the disease from South Africa by 1955 (Stoltsz, 1989; Lawrence et aI., 1994b; Uilenberg 1999). Although the disease has been totally eradicated, cattle in South Africa are still at risk of infection because the tick vector is still present in some parts of the country (Stoltsz, 1989; ILRAD, 1990).


January disease

January disease (also known as Zimbabwean theileriosis or malignant Rhodesian theileriosis) is a milder form of cattle-associated theileriosis that emerged in Zimbabwe after the eradication of classical ECF (Uilenberg, 1999). The symptoms of January disease are similar to but milder than those of ECF, and the two diseases can only be distinguished by seasonality. January disease is highly seasonal (occurs between December and March), with high mortalities in January which coincide with the availability of the tick host (Uilenberg, 1999). The causative agent was previously known as T parva bovis. There is no evidence of the occurrence of January disease in South Africa (Stoltsz, 1989).

Corridor disease

Corridor disease is the buffalo-associated form of the disease which still persists in most southern African countries, including South Africa (the causative agent was previously known as T parva lawrencei) (Lawrence, 1992). The parasite does not cause disease in the African buffalo reservoir host, but it can be transmitted from buffalo to cattle by infected ticks. It is thought that this form of the parasite is not transmitted between cattle, as infected cattle usually die before piroplasms appear or are too few to infect new ticks (Uilenberg, 1999). The clinical symptoms are similar to those of ECF, except that death usually occurs within a short time after the onset of the first symptoms (Lawrence et ai., 1994c). It is therefore regarded as a self-limiting disease in cattle (Norval et ai., 1992). However, cattle infected by buffalo-derived T parva can recover from infection after treatment by chemotherapy and become carriers of the parasite which are capable of infecting susceptible cattle (Potgieter et ai., 1988).

The epidemiology of Corridor disease in South Africa

Corridor disease has become the most important form of theileriosis in South Africa after the eradication of ECF as it poses a threat to the cattle farming industry in this country (Stoltsz, 1989).The disease was first recognized in the ‘corridor’ between the then Hluhluwe and Umfolozi (now Hluhluwe-iMfolozi) game reserves in the KwaZulu-Natal province of South Africa (Neitz et ai., 1955; Lawrence et aI., 1994a) and is currently endemic in the Kruger National Park (KNP) and in the Hluhluwe-iMfolozi game park, as well as in adjacent farms where cattle and buffalo are in close contact (Collins et aI, 2002; Mashishi, 2002).
Measures used to control Corridor disease in South Africa include the prevention of contact between cattle and buffalo, regular dipping and spraying of all cattle in disease-infected areas and testing of buffalo for theileriosis (and other controlled diseases) before translocation (South African Animal Disease Act 35 of 1984). However, despite all these strict control measures, sporadic outbreaks of the disease still occur in the country. In 1994, an outbreak of Corridor disease occurred in Warmbaths, Limpopo province, as a result of an illegal translocation of buffalo from an endemic area near the Kruger National Park (Collins et aI., 2002). More recently, Thompson et aI. (2008) reported an outbreak of theileriosis on a farm near Ladysmith in the KwaZulu-Natal province which is outside the declared Corridor disease endemic area. Infected buffalo from a neighbouring farm were suspected as the source of infection to cattle.
The phenomenon of ‘transformation’ of buffalo-associated T. parva to cattle-associated T. parva after serial tick passages in cattle has been described in East Africa by Barnett and Brocklesby (1966) and Young and Purnell (1973). However, experiments aimed at determining whether transformation can occur in South African T. parva isolates were unsuccessful (Potgieter et aI., 1988; Norval et aI., 1991).

CHAPTER 1 General Introduction
1.1 Background
1.1.1 The importance of proper diagnosis and characterization of Theileria infections of buffalo in South Africa
1.2 Problem Statement
1.3 0 b j ectives of the study
1.4 Thesis overview
1.5 References
CHAPTER 2 Literature Review
2.1 Classification of Theileria spp
2.2 Life cycle of Theileria in cattle and tick vector
2.3 Theileria species of buffalo and cattle in Africa
2.4 Theileria parva (Theiler, 1904)
2.4.1 East Coast fever (ECF) The epidemiology of ECF in southern Africa
2.4.2 January disease
2.4.3 Corridor disease The epidemiology of Corridor disease in South Africa
2.4.4 Control of T parva Chemical control of ticks Immunization of cattle Subunit vaccines Chemotherapy
2.4.5 Diagnosis of T parva Conventional parasitological techniques Serological techniques Molecular biology techniques .
I. Conventional Polymerase Chain Reaction (PCR)
II. PCR -based hybridization assays
III. PCR-based RFLPs
IV. PCR -based LAMP assays
V. Quantitative real-time PCR (qPCR) assays
2.5 Benign and mildly pathogenic Theileria species of cattle and buffalo in South Africa
2.5.1 Theileria mutans (Theiler, 1906)
2.5.2 Theileria sp. (strain MSD) .
2.5.3 Theileria sp. (buffalo)
2.5.4 Theileria buffelilsergentilorientalis (Neveu-Lemaire, 1912; Yakimov and Dekhterven, 1930; Yakimov and Sudachenkov, 1931)
2.6 Molecular characterization and phylogeny of Theileria spp
2.7 References
CHAPTER 3 Identification of Theileria parva and Theileria sp. (buffalo) 18S rRNA gene sequence variants in the African buffalo (Syncerus caffer) in southern Africa
3.1 Abstract
3.2. Introduction
3.3. Materials and Methods
3.3.1 Blood samples and DNA extraction
3.3.2 PCR amplification and reverse line blot (RLB) assay
3.3.3 Amplification, cloning and sequencing of the 18S rRNA gene
3.3.4 Phylogenetic analysis
3.3.5 Real-time PCR
3.3.6 Nucleotide sequence accession numbers
3.4 Results
3.4.1 RLB Results
3.4.2 Sequencing and phylogenetic results
3.4.3 T. parva real-time results
3.5. Discussion
3.6 References
CHAPTER 4 Sequence variation in the 18S rRNA gene of Theileria mutans and Theileria velifera isolated from the African buffalo (Syncerus caffer)
4.1 Abstract
4.2 Introduction
4.3 Materials and Methods
4.4 Results
4.5 Discussion
4.6 S ummary
4.7 References
CHAPTERS Sequence variation and molecular phylogeny of novel Theileria buffeli-like and Theileria sinensis-like genotypes of the African buffalo (Syncerus caffer) based on their 18S rRNA gene and internal transcribed spacer (ITS) sequences
5.1 Abstract
5.2 Introduction
5.3 Materials and Methods
5.4 Results .
5.5 Discussion
5.6 Conclusion
5.7 References
CHAPTER 6 Sequence variation in the V 4 hypervariable region of the 18S rRNA gene of Theileria spp. of the African buffalo (Syncerus caffer) and cattle: Implications for the diagnosis of Theileria parva infections in cattle and buffalo in South Africa
6.1 Abstract
6.2 Introduction
6.3. Materials and Methods
6.4. Results
6.5. Discussion
6.6 References
CHAPTER 7 Evaluation of a « pan » FRET real-time PCR test for the discrimination of Theileria species in the African buffalo (Syncerus caffer)
7.1 Abstract
7.2 Introduction
7.3 Materials and methods
7.4 Results
7.5 Discussion and Conclusion
7.6 References
CHAPTER 8 General Discussion, Conclusions and Recommendations
8.1 Identification and molecular characterization of pathogenic, mildly pathogenic and benign Theileria spp. of the South African buffalo
8.2 Molecular characterization and phylogeny of T. buffeli-like and T. sinensis-like genotypes of the African buffalo (Syncerus caffer) based on their 18S rRNA gene and internal transcribed spacer (ITS) sequences
8.3 Evaluation of the cox III qPCR assay for the simultaneous identification and differentiation of Theileria spp. in buffalo
8.4 References

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