Cattle transhumance in West Africa : risks associated with ticks and tick-borne pathogens dissemination and their zoonotic implications assessment

Abstract

In West Africa, livestock production represents an important part of the country's economy and the daily life of the population. The livestock production system is generally extensive, with low inputs, and based on the freely accessible natural resources exploitation. As a result, cross-border transhumance has become a real animal production strategy, leading to the mixing of herds in common pastures and around common watering points. Such situation favors potential exchanges of exoparasites such as ticks, vectors of numerous pathogens inducing infections (babesiosis, theileriosis, anaplasmosis, cowdriosis), constituting a major constraint to the livestock industry's development. In Burkina Faso (BF) and Benin (BN), these animal exchanges are particularly important at the eastern and northern borders respectively, which remain poorly explored localities despite the context of invasion of the two countries by Rhipicephalus microplus. The aim of this thesis is to analyze tick infestation in livestock, through the identification of the different species, the molecular characterization of transmitted pathogens and the evaluation of their zoonotic implications in the border areas of these two countries. Four studies were carried out : (i) a cross-sectional survey to study the epidemiology of ticks and associated pathogens in cattle, in order to characterize (ticks and hémoparasites) the eastern region of BF, the departure zone of transhumance, and the northern part of BN, the arrival zone, (ii) a longitudinal survey to evaluate the parasitological status (ticks and hemoparasites) of a sample of cattle over a transhumance season, (iii) a research of arboviruses circulating in eastern BF, (iv) a determination of the resistance status of two tick species (of veterinary interest) to commercial acaricide compounds, most commonly used by farmers in southwestern BF. Ticks and peripheral bovine blood were collected. Ticks were morphologically identified using a binocular magnifying glass. DNA extracts from both cattle blood and tick pools were analyzed by Reverse Line Blot Hybridization (RLB) process, followed by sequencing (Sanger method) for molecular detection of pathogens. Tick-borne viruses (arbovirus) characterization was performed by Next Generation Sequencing (Ion Torrent). Amblyomma variegatum and Rhipicephalus microplus resistance status to synthetic pyrethroids (deltamethrin and cypermethrin) was determined by Larval Packet Test (LPT). In the cross-sectional study, a total of 2,856 ticks (eight species) were collected from 490 cattle (46 herds) in eastern BF, while 3,583 ticks (nine species) were collected from 456 cattle (44 herds) in northern BN. Amblyomma variegatum was the most abundant and widely distributed tick species in both areas with a relative abundance of 49.2% in eastern BF, and 31% in northern BN. The R. microplus tick was not identified in the samples collected in eastern BF, but its expansion in others northern areas in BN was evidenced. Six tick-borne pathogens species were detected in cattle blood in both eastern BF and northern BN. The most prevalent were T. mutans (91.1%) and T. velifera (77.8%). Theileria annulata and T. velifera were detected for the first time in the study area. A total of 210 cattle were followed during the longitudinal study. A first sampling coded "T0BF" was implemented at the transhumance departure in eastern BF, a second sampling (T1BN) in the arrival area in northern BN, and a third sampling (T2BF) at the return of cattle in the eastern BF. A total of 1027 ticks (7 species), 1006 ticks (11 species) and 1211 ticks (9 species) were respectively found at T0BF, T1BN and T2BF. Some species were collected at the three times of sampling without any significant difference in their relative abundances. However, other tick species appeared only at T1BN and/or T2BF. The tick-borne pathogens (TBP) species found at the three points surveyed were T. annulata, Theileria mutans, T. velifera, Babesia bigemina and Anaplasma marginale. The most prevalent was Theileria mutans with 166/210 (79%), 159/210 (75.7%) and 78/210 (37%) cattle positive respectively at T0BF, T1BN and T2BF. The species Anaplasma centrale was highlighted for the first time in the area at T0BF and T2BF. A sample of ticks collected at T2BF (N=663) was tested for viruses and no arboviruses were detected. However, pseudocowpox virus (PCPV) (8.2%) and bovine papular stomatitis virus (BPSV) (5.8%) were evidenced in tick pools. The Rhipicephalus microplus strain tested showed resistance to deltamethrin and cypermethrin, with high lethal concentrations (LC), and resistance ratios (RR) higher than 4 (Deltamethrin: RR50= 28.18 and RR90 = 32.41; Cypermethrin: RR50 = 8.79 and RR90 = 23.15). On the contrary, the A. variegatum strain was very sensitive to the acaricides tested, with the lowest lethal concentrations and resistance ratios (Deltamethrin RR50 = 0.5 and RR90 = 0.48; Cypermethrin: RR50 = 0.68 and RR90 = 0.79). The diversity of tick species and the high prevalence of pathogens found in northern Benin indicate a higher parasite risk in this area compared to eastern Burkina Faso. As a result, herders in Burkina Faso expose their cattle to new tick species infestations, due to transhumance, which influence is combined with the seasonal variation of tick populations. In the rainy season, the recurrent use of trypanocides for both profilactic and curative care of animals, leads to a decrease in the prevalence of certain hemoparasites detected in cattle. The first detection of T. annulata, T. velifera and A. centrale species is a significant contribution to the knowledge of tick-borne pathogens in BF and BN. The discovery of PCPV and BPSV in ticks highlights viral zoonotic risks associated with cattle breeding in eastern BF. Furthermore, the resistance of R. microplus to synthetic pyrethroids indicates that the inefficiency of some acaricide molecules in tick populations control remains a concern in BF. Some of these results can be used as guidelines for the development of effective control protocols against ticks and transmitted pathogens, while others open new research lines, which, when explored, will enable a better understanding of tick spreading phenomenon and livestock infestation process.Appui aux réseaux d’épidémiosurveillance des maladies animales et aspects sociologiques associés en Afrique de l’Oues