Abstract
BackgroundTheileria parva causes East Coast fever (ECF), one of the most economically important tick-borne diseases of cattle in sub-Saharan Africa. A live immunisation approach using the infection and treatment method (ITM) provides a strong long-term strain-restricted immunity. However, it typically induces a tick-transmissible carrier state in cattle and may lead to spread of antigenically distinct parasites. Thus, understanding the genetic composition of T. parva is needed prior to the use of the ITM vaccine in new areas. This study examined the sequence diversity and the evolutionary and biogeographical dynamics of T. parva within the African Great Lakes region to better understand the epidemiology of ECF and to assure vaccine safety. Genetic analyses were performed using sequences of two antigen-coding genes, Tp1 and Tp2, generated among 119 T. parva samples collected from cattle in four agro-ecological zones of DRC and Burundi.ResultsThe results provided evidence of nucleotide and amino acid polymorphisms in both antigens, resulting in 11 and 10 distinct nucleotide alleles, that predicted 6 and 9 protein variants in Tp1 and Tp2, respectively. Theileria parva samples showed high variation within populations and a moderate biogeographical sub-structuring due to the widespread major genotypes. The diversity was greater in samples from lowlands and midlands areas compared to those from highlands and other African countries. The evolutionary dynamics modelling revealed a signal of selective evolution which was not preferentially detected within the epitope-coding regions, suggesting that the observed polymorphism could be more related to gene flow rather than recent host immune-based selection. Most alleles isolated in the Great Lakes region were closely related to the components of the trivalent Muguga vaccine.ConclusionsOur findings suggest that the extensive sequence diversity of T. parva and its biogeographical distribution mainly depend on host migration and agro-ecological conditions driving tick population dynamics. Such patterns are likely to contribute to the epidemic and unstable endemic situations of ECF in the region. However, the fact that ubiquitous alleles are genetically similar to the components of the Muguga vaccine together with the limited geographical clustering may justify testing the existing trivalent vaccine for cross-immunity in the region.
Highlights
Theileria parva causes East Coast fever (ECF), one of the most economically important tick-borne dis‐ eases of cattle in sub-Saharan Africa
The 405-bp sequence region of Tp1 encodes 134 amino acids (25% of the 543 amino acids of the full-length Tp1 gene). This region is located between nucleotides 537 and 941 of the reference genome of the T. parva Muguga strain (GenBank: XP_762973), while the 504-bp region of the Tp2 gene encodes 167 amino acids of the 174 amino acid-long protein encoded by the reference T. parva Muguga genome (GenBank: XP_765583)
We conducted a comprehensive analysis of Tp1 and Tp2 sequences to investigate the extent of diversity, the phylogenetic relationships and the evolutionary dynamics of T. parva samples obtained from cattle in four agro-ecological zone (AEZ) in the African Great Lakes region and determine how they relate to vaccine stocks and published sequences from various geographical areas of sub-Saharan Africa
Summary
Theileria parva causes East Coast fever (ECF), one of the most economically important tick-borne dis‐ eases of cattle in sub-Saharan Africa. A live immunisation approach using the infection and treatment method (ITM) provides a strong long-term strain-restricted immunity It typically induces a tick-transmissible carrier state in cattle and may lead to spread of antigenically distinct parasites. It has been demonstrated that ITM vaccination induces strain-specific immunity, mediated by the major histocompatibility complex (MHC) class I-restricted CD8+ T cells killing T. parva-infected bovine host cells [17]. This suggests that the evolutionary dynamics of genetic diversity, which usually result in antigenic variation of parasites, enable T. parva to escape recognition by the host immune system [18, 19]. To reduce the risks of introducing foreign parasite strains, a comprehensive study of parasite genotypes circulating in the region is required prior to the deployment of a live vaccine
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