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

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

Cattle ticks and associated tick-borne pathogens in Burkina Faso and Benin: Apparent northern spread of Rhipicephalus microplus in Benin and first evidence of Theileria velifera and Theileria annulata

peer reviewedBabesiosis, theileriosis, anaplasmosis, and heartwater are tick-borne diseases that threaten livestock production in sub-Saharan Africa including Burkina Faso and Benin. For over a decade, these two bordering countries have been facing an invasion of the livestock by the tick Rhipicephalus microplus, a major vector for babesiosis, accidentally introduced in Benin in 2004. The molecular identification of tick-borne pathogens in this border area is of particular interest due to animals seasonal migration between the two countries. In this survey, epidemiological features of ticks and tick-borne pathogens in cattle were investigated to compare the eastern Burkina Faso, corresponding to a seasonal migration departure zone, and the northern Benin, which represents a seasonal migration arrival zone. Ticks and peripheral blood were collected from a total of 946 cattle in the two areas. Ticks were morphologically identified and the DNA samples from bovine blood and ticks were analysed by Reverse Line Blot (RLB) hybridization process. A total of 2856 ticks were collected on 490 cattle in Burkina Faso, eight tick species were identified, while 3583 ticks were collected on 456 cattle in North Benin with nine tick species identified. The invasive tick, R. microplus was not found in eastern Burkina Faso, but its spread farthest north in Benin is reported. Six tick-borne pathogen species were found in cattle blood both in eastern Burkina Faso and in northern Benin. Ranked in decreasing order of overall prevalences, they are: Theileria mutans (91.1%), Theileria velifera (77.8%), Babesia bigemina (10.9%), Anaplasma marginale (4.2%), Babesia bovis (3.3%), and Theileria annulata (1.8%). To the best of our knowledge, this survey represents the first report of T. velifera and T. annulata in the region. Overall, the TBP prevalences were significantly higher in northern Benin than in eastern Burkina Faso, indicating a higher parasitological risk in this area. © 2021 Elsevier Gmb

Models for studying the distribution of ticks and tick-borne diseases in animals : a systematic review and a meta-analysis with a focus on Africa

Peer reviewe

Cross border transhumance involvement in ticks and tick-borne pathogens dissemination and first evidence of Anaplasma centrale in Burkina Faso

In West Africa, cross-border transhumance, also called seasonal migration, is known to be a very important animal production strategy, as it involves about 70 to 90% of cattle. In spite of the cattle movements, some strategic areas of transhumance remain poorly explored regarding ticks and their associated pathogens investigations. The purpose of this study is to evaluate the involvement of transhumance in the spread of cattle ticks and associated pathogens in Burkina Faso (BF) and Benin (BN), in a context of speedy invasion of West African livestock by Rhipicephalus microplus. A longitudinal survey was performed on 210 cattle from BF, monitored for ticks and tick-borne pathogens (TBP) during one seasonal transhumance. The first sampling coded “T0BF” took place in eastern BF, at the transhumance departure. A second sampling “T1BN” was carried out in northern BN, the transhumance arrival zone. A third sampling “T2BF” was done at the return of cattle in eastern BF. Ticks were morphologically identified and TBP detected with reverse line blot hybridization (RLB) assay. 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 TBP species found at the three points surveyed were Theileria annulata, Theileria mutans, Theileria velifera, Babesia bigemina and Anaplasma marginale. The most prevalent was T. mutans with 166/210 (79%), 159/210 (75.7%) and 78/210 (37%) cattle positive respectively at T0BF, T1BN and T2BF. Anaplasma centrale was evidenced with 0.5% and 0.9% respectively at T0BF and T2BF. To our knowledge, this represents its first report in the study area. Overall, the TBP prevalences were significantly lower at T2BF, highlighting the effect of tick populations changes induced by transhumance combined with the seasonal variation influence. © 202

First tick and tick damage perception survey among sedentary and transhumant pastoralists in Burkina Faso and Benin.

BACKGROUND: Transhumance, a main ancestral animal production strategy of the West African Countries (WAC), can favour the spread of vectors and vector-borne diseases within and/or across countries. Transhumance has been implicated in such spread as well as that of related tick-borne diseases (TBD). METHODS AND PRINCIPAL FINDINGS: Using a questionnaire survey and statistical modelling, this study explores the perception of herders about ticks and TBD in cattle, their practices in tick control and the social groups involved in cattle farming in eastern Burkina Faso (46 random herds) and in the northern Benin (44 random herds). Results show that most of the herders (79%) are from the Fulani social group. The principal and secondary activities of herders are respectively cattle farming and agriculture. The mean age of pastoralists is between 40 and 50 years depending on the province of origin and 60% of the surveyed herds practice internal or transboundary transhumance. Herders have a clear knowledge of different genus of ticks except the genus Rhipicephalus. Their knowledge of TBD is very limited. These results also reveal that herders in Benin use less acaricides treatment calendar compared with those in Burkina Faso. Transhumant pastoralists (i.e. transhumant cattle farmers) plan more acaricide treatment and have more cows with lost teats (i.e. tick damage) than the sedentary ones. In addition, amitraz appears to be the main acaricide compound used by herders for tick control (68%) but its use is inappropriate and its source is frequently the unregulated market. CONCLUSIONS AND SIGNIFICANCE: All of these findings can induce acaricide resistance especially as the inefficacy of amitraz against Rhipicephalus (Boophilus) microplus has already been reported in previous studies. Such results would help to elaborate suitable strategies of control and prevention of ticks and TBD in Burkina Faso and Benin

First digital characterization of the transhumance corridors through Benin used by cattle herds from Burkina Faso and associated risk scoring regarding the invasion of Rhipicephalus (Boophilus) microplus.

BACKGROUND: Livestock plays a key role in the macro economy of West Africa and provides livelihoods for millions of people. The main cattle rearing strategy in West Africa is pastoralism, including transhumance: i.e. a seasonal migration of cattle with their herders. This adaptive strategy aims to optimize livestock access to water and pastures. However, it can favour pathogens and vectors transboundary spread. This study aim is to highlight, firstly the corridors and grazing areas used by Burkina Faso transhumant cattle herds going to Benin, secondly the characteristics of departure and arrival areas of transhumance and thirdly, the risk score related to introduction and spread of the invasive tick species, Rhipicephalus (Boophilus) microplus, in free areas. METHODS AND PRINCIPAL FINDINGS: Therefore, GPS devices were given to 27 herders to monitor a full transhumance season between East Burkina Faso and North Benin. The analysis of 14,966 spots generated by the GPS devices revealed four main corridors and five main grazing areas used by cattle herds during transhumance. Statistical analysis of normalized difference vegetation index (NDVI), rainfall and temperature data, highlighted significant differences between departure and arrival areas. NDVI and rainfall are significantly higher in Benin than Burkina Faso whereas temperature is significantly lower. Additionally, using biotic and abiotic parameters, a risk scoring was developed to predict the presence of Rhipicephalus (Boophilus) microplus at municipality level. CONCLUSIONS AND SIGNIFICANCE: The better vegetation, temperature and rainfall conditions during the dry seasons in Benin attract cattle herds from Burkina Faso. The invasiveness and adaptability of Rhipicephalus (Boophilus) microplus added to the frequent stays of transhumant herds in infested areas suggest its potential introduction and establishment in free areas soon. Moreover, frequent intrusions of the transhumant cattle in the wildlife reserves is another risk of vectors and pathogen exchange between domestic and wild animals

Efficacy of two commercial synthetic pyrethroids (cypermethrin and deltamethrin) on Amblyomma variegatum and Rhipicephalus microplus strains of the south-western region of Burkina Faso

Since 2011, period of the livestock invasion by the cattle tick Rhipicephalus microplus in Burkina Faso (BF), tick-control problems were exacerbated. Based on farmer’s reports, most commonly used commercial acaricides were found to be ineffective in Western South part of the country. To investigate the occurrence and extent of such acaricidal ineffectiveness, we performed the standardized larval packet test (LPT) with commercial deltamethrin (vectocid) and cypermethrin (cypertop), on two cattle tick species, the native Amblyomma variegatum and the invasive R. microplus. The resistance ratios (RR) were computed with susceptible Hounde strain of Rhipicephalus geigyi as reference. The R. microplus population showed resistance to the two acaricides tested with the highest lethal concentration (LC) values, and different resistance ratios higher than 4 (deltamethrin: RR50 = 28.18 and RR90 = 32.41; cypermethrin: RR50 = 8.79 and RR90 = 23.15). In the contrary, A. variegatum population was found to be highly susceptible to acaricides tested with low lethal concentrations and resistance ratio values (deltamethrin: RR50 = 0.5 and RR90 = 0.48; cypermethrin: RR50 = 0.68 and RR90 = 0.79). These data demonstrate high synthetic pyrethroid resistance in R. microplus strain, leading to conclude that the acaricide ineffectiveness in tick populations control remains a concern in BF. © 2021, The Author(s)

Modelling habitat suitability of the invasive tick Rhipicephalus microplus in West Africa.

peer reviewedTicks have medical and economic importance due to their ability to transmit pathogens to humans and animals. In tropical and sub-tropical countries, tick-borne diseases (TBD) are among the most important diseases affecting livestock and humans. The fast spread of ticks and TBD requires a quick development and application of efficient prevention and/or control programs. Therefore, prior investigations on TBD and related vectors epidemiology, for instance, through accurate epidemiological models, are mandatory. This study aims to develop models to forecast suitable habitat for Rhipicephalus microplus distribution in West Africa. Tick occurrences were assembled from 10 different studies carried out in six West African countries in the past decade. Six statistical models (maximum entropy in a single model and generalised linear model, generalised additive model, random forest, boosted regression tree and support vector machine model in an ensemble model) were applied and compared to predict the habitat suitability of R. microplus distribution in West Africa. Each model was evaluated with the area under the receiver operating characteristic curve (AUC), the true skill statistic (TSS) and the Boyce index (BI). The selected models had good performance according to their AUC (above .8), TSS (above .7) and BI (above .8). Temperature played a key role in MaxEnt model, whereas normalised difference vegetation index (NDVI) was the most important variable in the ensemble model. The model predictions showed coastal countries of West Africa as more suitable for R. microplus. However, some Sahelian areas seems also favourable. We stress the importance of vector surveillance and control in countries that have not yet detected R. microplus but are in the areas predicted to host suitable habitat. Indeed, awareness-raising and training of different stakeholders must be reinforced for better prevention and control of this tick in these different countries according to their status