Genetic and antigenic variation of the bovine tick-borne pathogen Theileria parva in the Great Lakes region of Central Africa

Gaston S. Amzati, Appolinaire Djikeng, David O. Odongo, Herman Nimpaye, Kgomotso P. Sibeko, Jean-Berckmans B. Muhigwa, Maxime Madder, Nathalie Kirschvink, Tanguy Marcotty

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Abstract

Background
Theileria 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.
Results
The 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.
Conclusions
Our 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.
Original languageEnglish
Article number588 (2019)
JournalBMC Parasites & Vectors
Volume12
Issue number1
DOIs
Publication statusPublished - 16 Dec 2019

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Great Lakes Region
Theileria parva
Central Africa
Antigenic Variation
Ticks
Theileriasis
Vaccines
Alleles
Immunity
Nucleotides
Burundi
Tick-Borne Diseases
Antigens
Carrier State
Gene Flow
Africa South of the Sahara
Population Dynamics
Infection
Cluster Analysis
Epitopes

Keywords

  • Tick-borne diseases
  • East Coast fever
  • Muguga cocktail vaccine
  • Rhipicephalus appendiculatus
  • Population genetics
  • Tp1
  • Tp2
  • Evolutionary dynamics
  • Agro-ecological zones

Cite this

Amzati, Gaston S. ; Djikeng, Appolinaire ; Odongo, David O. ; Nimpaye, Herman ; Sibeko, Kgomotso P. ; Muhigwa, Jean-Berckmans B. ; Madder, Maxime ; Kirschvink, Nathalie ; Marcotty, Tanguy. / Genetic and antigenic variation of the bovine tick-borne pathogen Theileria parva in the Great Lakes region of Central Africa. In: BMC Parasites & Vectors. 2019 ; Vol. 12, No. 1.
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title = "Genetic and antigenic variation of the bovine tick-borne pathogen Theileria parva in the Great Lakes region of Central Africa",
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.",
keywords = "Tick-borne diseases, East Coast fever, Muguga cocktail vaccine, Rhipicephalus appendiculatus, Population genetics, Tp1, Tp2, Evolutionary dynamics, Agro-ecological zones",
author = "Amzati, {Gaston S.} and Appolinaire Djikeng and Odongo, {David O.} and Herman Nimpaye and Sibeko, {Kgomotso P.} and Muhigwa, {Jean-Berckmans B.} and Maxime Madder and Nathalie Kirschvink and Tanguy Marcotty",
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Genetic and antigenic variation of the bovine tick-borne pathogen Theileria parva in the Great Lakes region of Central Africa. / Amzati, Gaston S.; Djikeng, Appolinaire; Odongo, David O.; Nimpaye, Herman; Sibeko, Kgomotso P.; Muhigwa, Jean-Berckmans B.; Madder, Maxime; Kirschvink, Nathalie; Marcotty, Tanguy.

In: BMC Parasites & Vectors, Vol. 12, No. 1, 588 (2019), 16.12.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Genetic and antigenic variation of the bovine tick-borne pathogen Theileria parva in the Great Lakes region of Central Africa

AU - Amzati, Gaston S.

AU - Djikeng, Appolinaire

AU - Odongo, David O.

AU - Nimpaye, Herman

AU - Sibeko, Kgomotso P.

AU - Muhigwa, Jean-Berckmans B.

AU - Madder, Maxime

AU - Kirschvink, Nathalie

AU - Marcotty, Tanguy

PY - 2019/12/16

Y1 - 2019/12/16

N2 - 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.

AB - 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.

KW - Tick-borne diseases

KW - East Coast fever

KW - Muguga cocktail vaccine

KW - Rhipicephalus appendiculatus

KW - Population genetics

KW - Tp1

KW - Tp2

KW - Evolutionary dynamics

KW - Agro-ecological zones

U2 - 10.1186/s13071-019-3848-2

DO - 10.1186/s13071-019-3848-2

M3 - Article

VL - 12

JO - BMC Parasites & Vectors

JF - BMC Parasites & Vectors

SN - 1756-3305

IS - 1

M1 - 588 (2019)

ER -